Constancea 83, 2002
University and Jepson Herbaria
P.C. Silva Festschrift

Evolutionary and Ecological Implications of Plastic Responses of Algae

Eduardo A. Morales,1 Francis R. Trainor,2 and Carl D. Schlichting2
1Patrick Center for Environmental Research,
Academy of Natural Sciences of Philadelphia, PA 19103-1101, USA
2Ecology & Evolutionary Biology,
University of Connecticut, Storrs, CT 06269-3043, USA

Spines connecting Fragilarioid diatoms


On November 20, 1962 when Paul Silva was editor of the then new journal, Phycologia, the junior author and R. L. Hilton, both from the University of Connecticut, submitted a paper entitled “Pleomorphism in Scenedesmus longus”. By return mail, no e-mail at that time, Paul wrote: “The manuscript has been sent to reviewers, and although I could be mistaken, from a brief glance I should judge that their general reaction will be favorable.” We were certainly encouraged by this support.

In just a few weeks we learned that three reviewers took a rather different view, for on January 8, 1963 Paul wrote a second time: “I stand overruled.” Of course the next step was to revise the manuscript and resubmit, but the paper was eventually withdrawn.

We provide this bit of history to point out that when later published in the Bulletin of the Torrey Botanical Club (1963) as “Culture of Scenedesmus longus”, this article became one of the first of many papers from our laboratory dealing with the complex phenotypic expression in a genus, which has recently been divided into Scenedesmus and Desmodesmus (An et al. 1999). Yes, we were appreciative of Paul's initial support, as well as the professional and sympathetic treatment we received from the editorial office. Again, thank you! In retrospect, this was valuable training for later drafting publications dealing with a controversial subject, phenotypic expression.


While undergoing development or maturing as individuals/populations, algae are subjected to changing environmental conditions. We are well aware of the ability of the individual genotype to produce alternative phenotypes; many morphologies have been reported for distinct taxa. Nonetheless there appears to be a common belief that the plastic response is a peculiarity restricted to just a few taxa, or that it is the exception and thus atypical. As a result, the implications for algal physiology, ecology, taxonomy, and conservation have been largely neglected. Recent studies on plasticity at the genetic and molecular levels in a broad range of organisms only confirm what many have anticipated: Organisms are not merely at the mercy of the environment, but have evolved mechanisms to deal with the constant selective pressures from their ever-changing surroundings (Darwin 1857, Schlichting and Pigliucci 1998).

Ironically, the study of phenotypic plasticity within phycology seems to predate contributions dealing with any other group of organisms. For example, the green algal genus Scenedesmus has been recognized as plastic since the mid 1800's. But the contributions of Grunow (1859), Wolle (1887), Chodat and Malinesko (1893), and Grintzesco (1902) were enveloped in controversy, criticism, and doubt (Smith 1916; see Schlichting and Bruton 1970, Trainor et al. 1971, and Shubert 1975, for further discussion on this topic). In addition Beijerinck (1890), Senn (1899), and Livingston (1900) reported similar phenomena in green algae related to Scenedesmus. Even though phycological research in this area has continued for decades to provide additional support, literature dealing with an evolutionary perspective has been sparse. Only recently, examples including green algae and cyanobacteria have been taken into account (Bell 1991, 1992, Graham and Wilcox 2000, Mazel and Marliere 1989).

In the last few years, experimental evidence for plasticity has increased dramatically. This information has been mainly produced by ecologists and evolutionary biologists interested in unraveling the processes by which organisms are able to cope with sudden changes in the habitats in which they thrive. The majority of this literature concentrates on the study of reaction norms, the set of potential phenotypes that a particular genotype can express in different habitat conditions. Note that interest in reaction norms has had a long tradition within evolutionary biology since Woltereck (1909) coined the term based on his experiments on daphnids. Woltereck's work, coupled with growing interest in the concepts of both genotype and phenotype (Weismann 1885, Johannsen 1911), led to the understanding of the phenotype as the ultimate consequence of gene expression along with the dependence of gene activity on environmental factors. Later, these concepts were fine tuned theoretically (Baldwin 1896, Goldschmidt 1940, Schmalhausen 1949) and confirmed experimentally (Waddington 1942, Clausen et al. 1948).

Before there was consideration of the implications of plasticity, in an ecological and evolutionary context, the neodarwinian evolutionary synthesis (Huxley 1942, Mayr and Provine 1980) attempted to explain the adaptation of organisms over long periods of time and at small spatial scales through the production of ecotypes (Turesson 1942). Ecotypes are genetically distinct sectors of a population adapted to local conditions with the potential of becoming a separate species provided some type of barrier impeding exchange of genes with the original population is present. Thus, the ecotypic adaptation theory disregards both the effect of environmental fluctuations on populations over short periods of time and the fact that plasticity can also be a mechanism for speciation (Pigliucci 1996, Schlichting and Pigliucci 1998). Neodarwinists lacked satisfactory explanations for the remarkable ability of certain organisms to disperse very rapidly (as happens with the majority of fresh-water algae), for why some species are spread over a wide geographical area and yet remain a cohesive group of interbreeding organisms, and most importantly, for the mechanisms determining the ability of some individuals to withstand marked shifts in habitat conditions (e.g., those occurring in coastal systems and temperate lakes).

Recently, novel biochemical techniques have elucidated the genetic and molecular mechanisms behind plastic responses (Pigliucci 2001, Schlichting and Pigliucci 1993, 1998, and references therein). It is now known, for example, that plasticity is simply a matter of a modification in the ability of a genotype to express a particular character. Such a modification may occur before or after a character has been expressed and it is always the response to a change in either intra or extracellular environments, or both. Exploration of genetic processes such as epistasis (whereby the expression of one character is linked to the expression of others) and pleiotropy (when a particular gene controls the functionality of others) has further contributed to the elucidation of plastic mechanisms at the genetic and molecular levels (Pigliucci 2001, Pigliucci et al. 1996, Schlichting 1989).

Experimental evidence concerning phenotypic plasticity now seems so striking and unambiguous that widespread phenotypic stability can not be taken for granted. Yet some phycologists (e.g., Håkansson and Chepurnov 1999, Hegewald 1997, Round 1996) have reservations about the role of the environment in shaping the organism's phenotype --perhaps for historical reasons (Morales and Trainor 1997, 1999, Trainor and Morales 1999). As we shall elaborate later, two procedural factors seem to have been responsible for the failure to appreciate the role of phenotypic plasticity: the exclusive use of field collected and preserved material, as well as the use of standard conditions for the growth of organisms in the laboratory.

In an evolutionary sense, it has been repeatedly demonstrated that natural selection favors the evolution of plastic genotypes, since the unpredictability of the environment tends to suppress the production of an optimal phenotype (Wright 1931, 1932, Scheiner 1998). Thus, well-adapted organisms must be able to track environmental change and produce highly adapted morphs under a variety of environmental conditions. Indeed, plasticity can be adaptive as demonstrated in the predator-induced morphological changes in a plethora of organisms of diverse taxonomical affiliation, including the algae (Havel 1987, Lürling 1999). More recently, adaptive plasticity has also been discovered to be the response to physical environmental pressures (Gomez et al. 1995, Zirbel et al. 2000).

In the present review we attempt to place available information on algal plasticity in an evolutionary context and discuss the implications for other phycological fields. The merging of phenotypic plasticity data with current phycological thinking completely changes our view of algae as biological entities. It leads to an integrated species concept in which morphology, physiology, ecology, and evolution are intertwined. In addition, it helps us to understand the relationship between organisms and their immediate environment and how individuals can endure in constantly changing and even newly invaded habitats.

Phenotypic variation due to the environment: evolutionary and ecological considerations

The dissection of the sources of variation which account for the total phenotypic variability in an organism is difficult to accomplish with field populations. It is possible, however, to minimize variability by cultivation of live material under controlled laboratory conditions. Experimentation with clones, for example, makes possible the distinction between exclusively genetic and genotype-by-environment variability in a genetically homogeneous background. Other methodologies include the use of mutants (reviewed in Pigliucci 1996) with promising results in plants and cyanobacteria (Clack et al. 1994, Kehoe and Grossman 1996); and the characterization of protein and/or RNA molecules in environmentally induced phenotypes (Gutenbrunner et al. 1994).

Environmental effects upon the genetic machinery are brought about by various intracellular and extracellular factors operating throughout the life history of organisms. These factors elicit genetic responses that ultimately manifest themselves through a modification (physiological and/or morphological) of the phenotype. In other cases, as takes place with the green alga Scenedesmus, morphological and physiological changes are observed from parents to offspring (Morales and Trainor, 1999) (Fig. 1).

Genetic responses to environmental changes are coordinated through an epigenetic system capable of regulating the functioning of its parts (genes) (see reviews in Pigliucci, 2001, Pigliucci et al. 1996, and Schlichting and Pigliucci, 1998). The effect of such functioning is the “calibration” of an organism to the new surrounding conditions. Hence, many phenotypic characteristics are the end result of gene activity, with the amount and direction modulated by environmental variability.

The elucidation of the mechanisms underlying plastic responses is fairly recent, although some of the elements have been embedded in biological knowledge for some years. DNA research has revealed that not all the genetic information of an individual is used at one time, if it is used at all. In humans, for example, about 90% of the DNA has an uncertain function and remains inactive during the life time of an individual. Given the diversity of human cells, we can infer that for each cell type only a small portion of the total DNA will be functional. Genes that are not necessary for the expression of characters needed at a particular developmental stage, environmental condition, or to accomplish a particular function in the organism are “turned off”, but remain a part of the genotype. In more general terms, the environment triggers the expression of those regions in the DNA that provide the most appropriate characters required for survival at any particular time.

The process of turning genes on and off is known as gene regulation, and the resulting phenotypic variation is often marked and drastic (Levins 1968, Pigliucci et al. 1996, Schlichting and Pigliucci 1995, 1998, Stearns 1989). Gene regulation has been clearly illustrated in an environmental context in Calothrix (Mazel and Marliere 1989). When this marine cyanophyte is grown in media with low sulfur concentrations, it is still able to produce phycobilins by expressing a gene that codes for a phycobilin molecule composed of amino acids without sulfur.

A second type of genetic control of plasticity is allelic sensitivity, a process that produces gradual changes in the phenotype of an organism through a change in the amount and/or activity of a gene product (Schlichting and Pigliucci 1998). This mechanism is commonly known as acclimation, and it will be referred to as such in this text. For example, the process of chromatic adaptation, the capability of pigmented organisms to maximize photosynthesis in a fluctuating light environment, has been demonstrated to be under this type of genetic control. This is the case of the cyanophyte Fremyella diplosiphon which is able to maximize photosynthesis by production of different amounts of phycoerythrins and phycocyanins following changes in light quality (Kehoe and Grossman 1996). Recently, the molecular mechanism for chromatic adaptation has been connected with light sensing molecules closely related to phytochromes of higher plants (Yeh et al. 1997). Sensing molecules track changes in environmental light quality and then send the information (via a process still under study) to genes encoding the production of phycobiliproteins (Yeh et al. 1997). A similar mechanism has been found in Synechocystis sp. (Wilde et al. 1997).

Genetic vs. environmentally induced variability

Genetic sources of phenotypic variation include all those processes altering the structure and composition of the genetic material of an individual (mutations at the gene and chromosome levels, gene duplication, gene flow, and genetic drift). Such genetic sources (excluding mutations) especially apply to sexually reproducing populations, where genes are constantly sorted in new combinations, each ultimately yielding a novel phenotype. Natural selection acts on these phenotypes, leading to the survival of those that provide the maximum fitness, i.e., the best adapted to the conditions at hand.

On the other hand and as discussed previously, phenotypic changes due to environmental effects do not imply alterations in genetic structure and composition (mutations), but rather signal that different portions of the genetic code are expressed. The effects of this turning on and off of genes may, in some ways, be comparable to the appearance of novel traits by mutation (Goldschmidt, 1940), and may also produce adaptive phenotypes (Schaal and Leverich 1987, Via 1993, Via et al. 1995, and others).

Since in some cases the expression of characters is the mere product of gene action (i.e., without participation of the environment exterior to the cell), changes triggered by environmental cues have been traditionally referred to as “non-genetic”. This has contributed to the erroneous notion (sometimes termed Lamarckian) that the phenotype per se is able to respond to shifts in the external environment or medium (for a culture). It should be clear, however, that environmental factors operate over the genetic structure of an organism, a new physiological state is produced, and then a variant phenotype arises (Fig. 1). That is, there is always an underlying genetic action behind any phenotypic change.

Considering the rare occurrence of mutations and the small probability of their fixation by natural selection, phenotypic plasticity may be an important mechanism for adaptation and survival until genetic novelties appear. Asexual populations are considered to have less genetic diversity to counteract environmental changes. However, if plasticity is a property of their genetic complement, other alternative phenotypes may be “used” to cope with these changes (Levin 1988). Sexually reproducing organisms are also plastic, and genetic diversity within a species results in genetic variation for plasticity in the population (Scheiner 1998, Schlichting 1986, Via and Lande 1985). Therefore, each new recombinant may differ in its plastic response, providing the population with more opportunities (than in asexual populations) to withstand environmental demands.

Fine grained variation: acclimation, plasticity in a single organism

Habitat changes may frequently affect an organism during its lifetime. Such “fine grained” variations (MacArthur and Levins 1967) can be met by acclimation. Acclimation constitutes a form of phenotypic plasticity at the individual level and may be explained by means of normal curves depicting the physiological tolerance of organisms to environmental conditions (Morales and Trainor 1997). A physiological response by acclimation involves an adjustment to habitat conditions within the range of tolerance imparted by functioning genes. That is, there is an adjustment in the activity of genes that are already expressed (e.g., increased amounts of a specific protein might be produced).

For example, Sorokin and Krauss (1962), studied the effects of light intensity and temperature on cellular growth of Chlorella pyrenoidosa in synchronized cultures. Data were collected before cell division occurred, so the recorded changes in cellular material correspond to variations within a single generation of individuals. Temperatures above 15°C produced a wide range of doublings of cell material per day. At 40°C for example, the number of divisions varied from 3, at less than 125 µmol m2s-1 illumination, up to 13 doublings at approximately 750 µmol m2s-1. In contrast, temperatures below 15°C limited cellular growth due to increased decomposition of chlorophyll molecules.

Another example has been provided by Ben-Amotz (1975) from experimentation with Dunaliella parva, an alga that is able to persist in highly saline waters. Again in this case, variations in intracellular osmotic water content were recorded before the organism was able to divide. Even just 5 min after the exposure of cells to increased salinity, a dramatic decrease in the osmotic water content was observed. Under these “non-metabolic” conditions (photosynthesis is negligible in such short time periods), glycerol content in the cell remained constant enabling the cell to maintain an osmotic equilibrium with the external medium. In the long term and when photosynthesis was operating, osmoregulation depended on the synthesis (through photosynthesis or metabolic degradation of starch) or degradation of glycerol. Cells incubated for periods of about 90 min at 25°C showed an increased glycerol content and a constant content of osmotic water throughout the period.

Even though there are numerous other examples among the microalgae, we believe that several are best discussed as typical of adaptation to “coarse grained” variation in the external environment (see later). For investigational studies of acclimation in the algae, macroalgae, especially seaweeds, have been more useful experimental organisms than microalgae (Dawes et al. 1976, Fain and Murray 1982, Mathieson and Burns 1971, Ogata 1966, among many others).

Heterophylly in aquatic emergent angiosperms constitutes an example of how individuals exhibiting continuous growth (also called modular organisms) are able to change their appearance during their lifespan. It has been proposed that heterophylly may be the outcome of at least two mechanisms (Winn 1996). First, the production of different phenotypes is the result of a developmental pathway that is already programmed in the genotype. This process, known as heteroblastic development, does not depend on external environmental influences, and has been demonstrated for some aquatic plants (Arber 1919, 1972, Kaplan 1980). The second mechanism, and the one that concerns us in the present paper, is plasticity itself (Young et al. 1995), the response to environmental variation leading to morphological changes in successively produced leaves. Experiments have demonstrated that the switch from an aquatic to aerial location, or from aquatic to terrestrial habitats, can lead to impressive changes in leaf physiology and appearance (Chabot and Chabot 1977, Cook 1968, Cook and Johnson 1968, Ku and Hunt 1973, among others). Such differences prove in many cases to be adaptive, improving the fitness of the organism to the new habitat state (see discussion presented by Schlichting and Pigliucci 1998).

Examples of heterophylly-like phenomena among the macroalgae have been studied for a number of years (Norton et al. 1981). Working in Pterocladia caerulescens, Santelices (1978) showed that the thallus of an individual alga exhibited morphological variation related to seasonal variations. Thus, while the summer thallus has an elongated and thin appearance, the winter thallus is broader and more robust. In other cases, shape modification can be more dramatic as it occurs in Fucus gardneri (Blanchette 1997), Hedophyllum sessile (Armstrong 1989), and Griffithsia pacifica (Waaland and Cleland 1972).

Conspicuous morphological changes can also be seen in microorganisms. In the case of the dinoflagellate Ceratocorys horrida (Zirbel et al. 2000), phenotypic alterations are triggered by a physical effect, e.g., turbulence. Cultures containing long-spined morphs, subjected to agitation in the laboratory, yielded populations composed of cells with much shorter spines. In a few of the cultured cells that particular modification in morphology occurred within an hour after agitation was initiated, and by 12 days ca. 70% of the individuals had developed short spines. Since growth rates were negligible during the morphological modifications and these occurred prior to the 16-day doubling time, morphological changes occurred within individuals. Zirbel et al. (2000) also demonstrated the ability to reverse this change of spine length, for cultures of short-spined cells, returned to static conditions, exhibited an almost complete phenotypic reversal in a period of 30 days. Although a small percentage of cells in all cultures remained spineless, further studies demonstrated their capability of quickly producing either the short or long-spined phenotypes.

Coarse grained variation: plasticity across generations

Variation in habitat conditions at intervals greater than the life span of individuals has been termed “coarse grained” variation (MacArthur and Levins 1967). In this case, changes in the environment trigger a mitotic cell division and the new phenotype is expressed in the filial generation. Most of the cases of plasticity in the phycological literature deal with this coarse-grained responses to environmental cues, for example, Phaeodactylum tricornutum, a pennate diatom, produces oval, fusiform, and triradiate morphs following changes in culture media, light, and temperature. This diatom was recognized as plastic in 1935 by Barker, and since then, various papers have been published on the DNA content, ultrastructural features, and biochemical characterization of the morphs (e.g., Borowitzka and Volcani, 1978, Darley 1968, Gutenbrunner et al. 1994, Lewin et al. 1958, Reimann and Volcani 1968).

A critical body of evidence concerning plasticity has been gathered for a variety of cyanobacteria, and through this evidence, taxonomic implications of plasticity have become very clear. The historical development of the classification of this group depicts very well a classic confrontation between “splitter” and “lumper” approaches. Early publications (Geitler 1932) presented extensive lists of organisms that were later complemented with additional descriptions of cyanophytes from other parts of the world (Cocke 1967, Desikachary 1959). The number of “species” was staggering, but it was not clearly stated whether the names were designed to represent different genotypes or strikingly different phenotypes. Subsequent collection of laboratory data on the plasticity of individual blue green algal genotypes led different authors to reduce drastically the number of taxa to be accepted.

Drouet and Daily (1956) for example, reduced the number of accepted names of coccoid forms from 2800 to just 32! Although most researchers criticize Drouet's conclusion, since it was based on examination of preserved material rather than on experimentation, later work with other cyanobacterial groups under controlled laboratory conditions has demonstrated extensive plasticity. Many of the characters used to separate species were found to be highly dependent on the conditions to which the organisms were subjected (e.g., Stein 1963, Foerster 1964, Robinson and Miller 1970, Sinclair and Whitton 1977). For the genus Spirulina for example, Jeeji-Bai and Sheshadri (1980) concluded that the degree of coiling of the trichomes (used to separate this genus from Arthrospira) varies with light intensity and nutrient concentration in the culture medium. Additionally, other “species” showed a wide spectrum of morphologies depending on both nutrient availability and the age of the material. In some cases, a single clone produced morphologies that could be placed within four different genera! Such was the case of Calothrix fuellerbornii, a species able to produce its own typical morphology, as well as Plectonema-like, Lyngbya-like, and Anabaena-like trichomes (Jeeji-Bai 1977). Recent molecular studies confirm that different cyanobacterial morphologies can be found in a single clade (Baurain et al. 2002).

A classic study on cyanobacterial plasticity was presented by Lazaroff and Vishniac (1961, 1964) and Lazaroff (1966), illustrating plastic responses of a strain of Nostoc muscorum. Morphological changes in this cyanophyte were triggered by differences in light intensity. A culture maintained in dark conditions always produced “aseriate” colonies, probably due to either a lack of essential substances for the formation of filaments, or by accumulation of inhibitory material. Under dim light conditions (0.2-0.9 µmol m2s-1), a transition from aseriate to filamentous forms was observed. In the range 16-90 µmol m2s-1 (still considerably less than full sun) typical filamentous forms were yielded. Furthermore, a culture containing aseriate colonies could be induced to produce filaments by adding an extract of a light-grown culture (Lazaroff and Vishniac 1961).

Spectral quality was also found to induce formation of different morphs in N. muscorum; cultures of aseriate forms maintained in red light produced filaments, but, green light triggered the production of aseriates from filamentous colonies. Allophycocyanin and one or various phycoerythrins were determined to be the photoreceptors for red and green light respectively (Lazaroff 1966). Although no attempts have been made to relate all these results to natural conditions, it would not be difficult to imagine changes in light intensity and spectral quality in bodies of water related to both position in the water column and seasonal changes. Broadly, we may hypothesize that during winter less light would be available to organisms because either day-length is short or the ice layer (in the temperate zone) would not allow deep penetration of light into the water column. Under these conditions one can expect to find large populations of aseriate colonies. During early summer, on the other hand, longer days and more red light are available to the organisms, resulting in production of filaments.

Salinity also plays a role in plastic responses of other cyanophytes. Stam and Holleman (1975) demonstrated that what were previously considered to be different freshwater species of Phormidium, in fact corresponded to morphs of a single genotype. These strains had the capability of changing their appearance back and forth when they were transferred to different media with variations in salinity. However, when such strains were cultured together under the same conditions, similar morphotypes were produced. Similarly, salinity has been demonstrated to trigger morphological changes in other organisms such as diatoms (e.g., Cox 1995, Schultz 1971).

Dispersion: the role of polymorphism and plasticity

Invasion of new habitats may also elicit novel physiological responses from genotypes. In the case of polymorphic populations, new habitats may lead to differentiation of ecotypes if a subset of organisms of a given species becomes locally adapted. For example, Yarish et al. (1979), working with the red alga Bostrychia radicans, established clonal cultures from the head and outlet of the Great Bay Estuary in New Jersey (USA) and subjected them to varying salinities in the laboratory. Compared to clones from the origin of the estuary, cultures from the outlet exhibited significantly higher growth rates at salinities of 15 0/00 and 25 0/00, when compared to growth at lower salinity (5 0/00). Such differential responses persisted even after storage of clones in reciprocal salinities for 2 years before the experiments. The same authors reported similar ecotypic differentiation in Caloglossa leprieurii.

On the other hand, the fate of plastic invading genotypes is far more complex. If the new environment is unstable, but the invading genotypes are sufficiently plastic to cope with these changes, then natural selection will favor them without any alteration in their genetic material. However, if the new habitat is substantially different from the original one, some of the plastic potential of these genotypes may be lost over time through genetic drift and/or modification of the epigenetic system (Schlichting and Pigliucci 1998). If the latter two processes are coupled with reproductive isolation from the main population, they might lead to speciation.

The fact that algal genotypes are able to adapt to their habitat through plasticity has been under-explored in evolutionary and phycological research. It is not difficult to conceive, however, that plasticity may be an important factor imparting fitness under changing environmental circumstances, and thus, confer on organisms at least a temporary resistance to evolutionary change (Bradshaw 1965, Sultan 1987). Many authors propose that it is the reaction norm itself which is the subject of natural selection. Genotypes that are able to produce a wider range of phenotypes and to cope more rapidly with changes in habitat conditions will be more apt to survive (Baldwin 1896, Bradshaw 1965, de Jong 1995, Gause 1947, Pigliucci et al. 1996, Scheiner and Lyman 1989, Scheiner 1993, Schlichting 1986, Stearns 1982, Via and Lande 1985).

Separation of polymorphic and plastic responses in natural populations is rather difficult (despite claims to the contrary [Mann 1999]), for a mixture of both processes often occurs in members of the population. Francke and Ten Cate (1980) working on populations of the chlorophyte Stigeoclonium tenue illustrated this point. Clones isolated from several sites in the Netherlands were subjected to varying concentrations of phosphorus, ammonia, and chloride. The clones exhibited dissimilar growth responses (Fig. 2). Not only did clones from different geographical areas respond differently (plasticity), but there were also differences between clones from the same locality (local polymorphism) . These data suggest that the species S. tenue is both plastic and polymorphic, and that over its range of distribution, some of its genotypes are locally adapted as shown by differences in growth rates between allopatric clones grown at similar nutrient concentrations. Phenotypic plasticity in S. tenue is not restricted to growth; conspicuous morphological changes also occur, and these have had taxonomic implications (Francke and Simons 1984, Campbell and Sarafis 1972).

Costs of plasticity and non-adaptive plasticity

As exposed above, species vary in their plastic capability, and even within a single population there are differences in plastic responses between genetically dissimilar individuals. Some of this inter and intraspecific polymorphism for plasticity may be due to the existence of constraints that impede the evolution of infinitely plastic genotypes (e.g., Gomulkiewicz and Kirkpatrick 1992, DeWitt 1998, DeWitt et al. 1998, Whitlock 1996). Besides the constraints imposed by the genetic structure of the organisms, there are costs to plasticity. These costs refer mainly to the difficulty of maintaining a “machinery” for plasticity, costs derived from the production of new phenotypes, and costs related to acquisition and utilization of information from the surrounding environment (DeWitt et al. 1998, Pigliucci, 2001, Schlichting and Pigliucci 1998). Pigliucci (2001) recognizes five types of costs of plasticity. First, costs involved in the maintenance of a genetic infrastructure capable of plastic responses. Second, costs related to the production of phenotypic characteristics by means of plastic mechanisms. Third, energetic costs linked to the acquisition of information from the surrounding environment. Four, the ability to modulate the phenotype implies a certain developmental instability, which leads to costs derived from a “developmental imprecision”. And finally, there are costs related to linkage, epistatic, and pleiotropic interactions of plastic genes. That is, plastic responses of a gene may have the detrimental consequences of the genes linked to it.

Accumulation of these costs can affect both the ecological performance of plastic organisms and their evolution. At the ecological level, an exaggerated cost of an adaptive plastic response may affect the competitive ability of an organism, favoring less plastic individuals that allocate more resources directly to reproductive fitness. Thus, even though plasticity may lead to the production of the most adequate phenotype in a given environment, such plasticity may not be selectively advantageous (DeWitt et al. 1998).

The effect of plasticity thinking on algal taxonomy

Several studies have demonstrated that morphological characters are not sufficient to define certain taxa (e.g., all the cases of morphological plasticity presented in this paper). Although the use of morphological characters provides a very convenient and practical way of classifying organisms, true affinities among individuals are not necessarily resolved by this approach. The problem might indeed have more serious repercussions than we first suspect. It is sometimes difficult to admit that additional data should be included in the classification of groups such as diatoms (Round 1996), when other facets of diatom research (e.g., paleolimnology) make extensive use of current morphological schemes. Diatom classification systems are largely based on description of acid cleaned material, on which further studies to unravel the source of phenotypic variation are practically impossible. It has been proposed that multivariate analyses of morphological features of diatom cell walls would enable researchers to uncover polymorphic vs. environmentally related variations in natural populations, thus, strengthening the use of morphology for delimitation of taxa (e.g., Theriot 1987). Although such studies indeed reveal morphological variation due to habitat differences, they fail to ascribe such variation to cases of plasticity or polymorphism simply because genetic data are not taken into account. Furthermore, such studies do not explore the role of other processes such as parallel evolution and canalization (see below) in the determination of diatom morphology. In any morphologically based system, consideration is not given to the possibility that morphological variation in allopatric situations can be due to polymorphism (i.e., morphs could correspond to locally adapted genotypes) and plasticity (i.e., morphs could be the result of gene regulation operating in one or more genotypes). Furthermore, in sympatric situations morphological variation could be due to genetic diversity within a single population and/or to plasticity due to existence of microhabitats within a single ecosystem. As shown previously, the extent to which polymorphism and plasticity contribute to the generation of phenotypic diversity within and among sites has been clearly illustrated for species of Stigeoclonium (Francke and ten Cate 1980) and there is no reason to doubt that this example is not applicable to the case of other sexually reproducing organisms.

Perhaps, even in the face of evidence, some researchers may still insist that the common “rule” in nature is the tendency for a genome to produce similar phenotypes when it is exposed to different environments (e.g., Håkansson and Chepurnov 1999, Round 1997). The maintenance of a phenotype under changing environmental conditions (canalization) is the result of stabilizing selection (Schmalhausen 1949, Waddington 1942). In general terms, canalization arises when a polymorphic population is subjected to a shift in the environment (e.g., seasonal changes in a lake) and a subsequent selection of genotypes producing optimal phenotypes under those conditions. Upon alteration in the sequence of habitat change (e.g., a prolonged drought in the lake), the capability of producing a particular morph will tend to be selected against, restricting a plastic genotype to the point of no plasticity. The observation of the occurrence of canalization in nature may have contributed to the establishment of the dogma on stability of form. However, we see canalization simply as an additional outcome of the interaction between the genotype and the environment. Unexposed portions of the reaction norm will be manifested in newly modified environments, and this reaction norm will be again diversified by sexual reproduction. Plasticity can not be merely “erased” from genotypes simply because genes within a genotype are always interacting with each other (see Schlichting and Pigliucci 1998 and references therein), and because adaptive plasticity is a character that will be maintained by natural selection. A second possibility for the pervasive use of a canalization argument in phycological literature could be related to the nature of sampling utilized in taxonomic studies. The majority of algal floras have been based on single collections for a locality at one or only a few points in time. This has contributed to the observation of only a small window in the life history of taxa (Trainor 1998).

With development of transmission electron microscopy (TEM) and molecular techniques, it becomes apparent that light microscopy (LM) and scanning electron microscopy (SEM) are not the only alternatives for description of new taxa. Modern approaches to classification, as shown by bacteriologists, could also include biochemical and physiological characteristics of organisms. Combination laboratory and field approaches would no doubt yield more accurate data regarding organismal relationships (Pringsheim 1967). The use of DNA and RNA sequencing in strains of Scenedesmus, for example, seems to be a key step in solving affinities within this genus (Hegewald 1997). More natural classification schemes would be produced by integration of multidisciplinary studies. LM and SEM become useful again when they are combined with TEM for the study of life cycles (reproduction, mitosis, cytokinesis), and morphological studies -including plasticity- on vegetative and reproductive cells (e.g., examining plastids, cell walls, flagella, etc.). These data paired with DNA, RNA, protein sequencing and allozyme analysis would no doubt yield a more reliable and objective algal taxonomy and systematics (Morales and Trainor 1997, Trainor and Morales 1999).

Will recognition of an ordered sequence decrease the number of species?

From the taxonomic standpoint, plasticity is often viewed as a process that--- if recognized or taken into account--- would reduce the number of species for a given genus, as former 'species' are recognized as morphs. In the case of Scenedesmus, for example, the morphs produced during the ordered sequence of development have in fact previously received variety and species designations (Hegewald and Silva 1988, Hegewald 2000). [Note: With strong support from molecular data the spine-bearing taxa are no longer placed in Scenedesmus, but rather in Desmodesmus, sometimes with little argumentation (Hegewald 2000)]. In both genera the inadequacy of numerous older protologues, and the need for emending them has become apparent. As the developmental sequence is incorporated into our understanding of the species, morphological similarity between two newly recognized sequences could lead one to believe that there is but one taxon (Table 1). As we examine this conclusion more closely, we would recognize that organisms might have morphological similarity coupled with marked physiological differences. Even the overall morphological similarity might yield fine texture differences, observed and enhanced under the SEM.

A concept of the genus

In the past we have used slices of a layered cake (Fig. 3) to represent diagrammatically some species in a plastic genus such as Scenedesmus (Trainor 1998). Note the recent proposal to remove the spine bearing scenedesmoids from Scenedesmus and place them in Desmodesmus (An et al. 1999); we refer to the complex as Scenedesmus/Desmodesmus. Given the unattainable task of presenting all variation possibilities, the slices composing the cake represent the average genotype of each species in the genus. As we assemble such a cake each morph of a Desmodesmus could be positioned in a separate layer, unicells on top, bicaudates in a lower layer. The picture becomes a bit cloudy when it is noted we sometimes have formerly separated species, e.g. D. bicaudatus, but yet included similar varieties in a taxon such as D. quadricauda var. bicaudatus!

When we use the concept of a layered cake for the genus, a typical cake slice (Fig. 3), incorporating several morphs such as A, B, C, D, E, is the species; many of the older 'species' or varieties from the literature simply become morphs. But in time, with the accumulation of more data, we would recognize that two adjacent cake slices, which at first sight appear morphologically identical, are often physiologically and reproductively very, very different. In some groups in which numerous varieties and forms have traditionally been recognized (Scenedesmus/Desmodesmus), the actual species diversity might remain low, but in these species we would have to recognize and incorporate numerous morphs.

In another example, a particular A B C D E slice might better be depicted as A B C D E, simply to point out the increase in thickness of one layer. In nature this readily identifiable morph might persist in the environment far longer than the similar morph for the rest of the species. Is this alteration due solely to environmental influences or because of a mutation? In time and with more data available we might recognize taxa for either option, both of which would be genetic, one because of gene regulation, the second due to mutation.

In the case of Scenedesmus/Desmodesmus (An et al. 1999), our hypothesis is that although at one time there were approximately 330 described species, with the recognition of plastic organisms the number will first be lowered considerably, perhaps even to 20 (Table 1). But then over time it will begin to increase, for, with new interpretations coupled with correction of obvious past mistakes, along with the use of plasticity data, the actual number might eventually approach 250, or more. How is this possible?

As we were alerted to, recognized, and made use of plasticity data with its sequence of development, the number was first lowered. But with additional characters, such as molecular and/or non-morphological data, we recognize that morphologically similar slices are indeed different taxa. In the end, considering our objectives thoroughly and employing a battery of stable characters, the number could steadily rise. But our understanding of each of these taxa, aided by emended protologues for each, will be very different. If we consider that adjacent cake slices might represent species that in reality are not closely related (determined by molecular information), the cake becomes a phylogenetic representation of members of a genus.

A concept of the species

In attempting to understand a species complex within a large genus, we might once again consider the model of a layered cake. And in order to avoid inevitable complications, initially only some members of the genus might be evaluated. Note that if the example were to be Scenedesmus/Desmodesmus one might be reluctant to incorporate many varieties and forms, simply because “far more taxa have been described than merit taxonomic recognition” (Silva in Hegewald and Silva 1988). The task would be full of twists and turns because a great many of the provisions of the International Code of Botanical Nomenclature would have to be considered. We would anticipate that a concerted cooperative effort would be essential.

We might first want to consider two adjacent cake slices in Figure 4. These may initially look identical, but understand that they exhibit polymorphism in their physiological, molecular, and perhaps even, in a limited sense, in some morphological characters. We might learn that they are sufficiently different so that interbreeding fails, or without reverting to the biological species concept, sufficiently different to express markedly different reaction norms. For Sellaphora pupula (=Navicula pupula) Mann (1989) pointed out that morphologically similar populations were actually reproductively isolated species, but we could always use more supporting data.

In the case of the diatom Fragilaria construens, several morphs of diverse morphology have been described and illustrated (Krammer and Lange-Bertalot 1991), and they have been assigned a variety or form status in some recent taxonomical reviews, while some have even been elevated to species! Although many diatomists have felt that studying the life cycle of diatoms may introduce new and more reliable criteria useful in diatom taxonomy (Cox 1996, Geitler 1968, among others), the more traditional morphologically based taxonomy still persists. The F. construens group includes a diversity of morphs that range from cruciate to triradiate to linear and elliptical. Yet it has not been determined whether there is a purely genetic or an environmental basis for such a diversity. Although it is premature to present a firm conclusion at this point, it is often the case that some of the morphs tend to be restricted to certain environmental conditions, whereas others are associated together under similar environmental circumstances. Whether these are genetically distinct and locally adapted segment of a species (varieties) or morphological variations induced by environmental change (forms) is simply not known.

Nevertheless one can hypothesize that a mixture of both processes is occurring simultaneously within the F. construens complex. Such a supposition can be based on both observations of field collected material and experimental work on closely related species. A well-developed population of F. construens was found in Avery Pond, a small eutrophic system located in southeastern Connecticut, USA (Morales 2001). Several morphological series were found in a surface sediment sample collected from this locality (Fig. 5). In each series, the nominal variety and the variety venter were found to exhibit similar characteristics, except for valve shape.

The first series (first column in Fig. 5) represents what is illustrated in the literature as the typical F. construens var. construens and F. construens var. venter. This series is characterized by a more or less narrow sternum, slightly elongated areolae composing the striae, spines located on the costae, and a few apical pores each surrounded by a rim located on both valve poles.

The second column (Fig. 5) represents a series with wider areolae, which are arranged in much shorter striae, delimiting a wide sternum on the valve face; the spines are also located on the costae. Some specimens in this series have well-developed apical pore fields on both poles of the valves, but again, a siliceous rim surrounds each individual pore.

Finally, the third series (third column in Fig. 5) is characterized by wide areolae arranged in striae that delimit a narrow sternum along the longitudinal axes of the valves. The spines lie on the costae between neighboring striae. Apical pore fields are also developed and located at both valve poles; a siliceous rim surrounds each individual pore.

Since the three series above seem to be closely related to each other, at least morphologically, they might represent genotypes within a single population. It is difficult to justify a variety status for the elliptical morphs for there seems to be a continuum of morphological characteristics with the cruciate morph. There is a distinct possibility that both morphs are expressions of even a single genotype subjected to microenvironmental differences in the same habitat. Hence, a mixture of polymorphism and plasticity could occur in this population.

If one observes material from additional ecosystems from North America and other parts of the world, many more morphological series can be found for the construens group (e.g., Rumrich et al. 2000). This means that the slice of the cake that represents F. construens is very generous, very thick! Each of the morphs within a series (cruciate or elliptical) will occupy a single layer in the cake. But are there more layers within a slice of F. construens?

There are at least two additional morphs exhibiting characteristics similar to those of the cruciate and elliptical types (Fig. 4). One is biundulate and has been described as a distinct variety, i.e., F. construens var. binodis, while the triradiate morph has been depicted as a separate species, namely Fragilaria exigua. The features of the areolae, spines and apical pore fields are similar in these four morphs, although apical pore fields might be extremely reduced or absent in the triradiate morph. It is very common to find a mixture of these morphs in field samples, although the triradiate morph tends to be more restricted in distribution. With these facts in mind, one might conclude that all morphs are related to each other and that they represent environmental variations of the same species. Thus a single genotype could produce all these morphs when subjected to a suite of environmental conditions. Therefore, each morph would be represented in but one layer in the cake (Fig. 4).

With the exploration of wider geographical areas, and intensive use of SEM we learn that several other fragilarioid 'species' also exhibit the above range of morphological variation (Krammer and Lange-Bertalot 1991, Rumrich et al. 2000). The F. brevistriata group, for example, also presents cruciate, elliptical, biundulate (even triundulate), and triradiate examples (Fig. 4, triundulate morph not shown), while those frustules associated with F. pinnata produce ellipsoid and triradiate morphs. Lastly, the F. leptostauron group includes cruciate, ellipsoid, and tetraradiate morphs (they would be positioned on the far right in Figure 4; only the elliptical morph is shown). With the experimental evidence presented by Schmid (1997) for F. crotonensis and Centronella reicheltii, we recognize that the cake analogy for fragilarioid taxa might be perfectly viable.

Schmid (1997) working with unialgal clones under controlled laboratory conditions showed that the change from linear to triradiate valves was reversible and depended on environmental conditions at the time of auxosporulation. This experiment remains one of the most elegant demonstrations of developmental plasticity, for we learn that the phenotype developed depends on the conditions under which the filial individuals are generated.


1. Phenotypic plasticity is the process by which a single genotype is able to produce different phenotypes when environmental conditions change. It is not an isolated phenomenon, restricted to certain taxa, but a widespread process among all organisms (including the algae). Phenotypic plasticity may be viewed as a way of maintaining fitness during changes in habitat conditions, and thus, as a way of buffering evolutionary change, making species less vulnerable to erratic climatic shifts (natural selection). Unwittingly, we have been considering plasticity in biology for a long time. Leaf dimorphism in aquatic macrophytes, chromatic adaptation in cyanobacteria, even cell differentiation in animals and plants, are some very well known examples that fit within the plasticity concept.

2. At times algal evolutionary, taxonomic, and ecological thinking does not incorporate sufficiently the concept of phenotypic plasticity. Perhaps we should no longer continue to think of many algal species as morphologically stable entities, since all genotypes may potentially be plastic and/or polymorphic. Our task is to ascertain the degree of plasticity and polymorphism in each one of them.

3. The implications of plasticity in other branches of phycological research (e.g., taxonomy and systematics) are obvious. Classification and identification should be based on analyses of as many types of traits as possible - the traditional morphological aspects as well as information on physiology, life histories, and even ultrastructural features, could provide important clues regarding organismal affinities. Considerations of phenotypic plasticity and polymorphism may significantly affect our view of phylogenetic relationships and classification schemes. In a number of cases, the use of laboratory techniques (e.g., culturing) is of utmost importance in the elucidation of plasticity, since they provide the opportunity to work with genetically homogeneous populations and environmentally homogeneous conditions. However, field and laboratory approaches must not be divorced from each other, for both may contribute to the establishment of true links among organisms. The adoption of either of these approaches to the exclusion of the other may lead to serious error. The development of more natural classification systems should now incorporate multidisciplinary considerations, including phenotypic plasticity and polymorphism.


In the absence of consensus, we provide the following definitions. At present our goal is simply to allow us the opportunity to record and communicate the full range of variation.
The ability of a single organism to adjust its physiology in order to meet environmental changes. Conceptually, it represents plastic responses that do not result from the activation of different genes, but from modulation of genes already expressed (see allelic sensitivity).
Allelic sensitivity
A mechanism of phenotypic plasticity by which there is a modification in the function of an expressed gene. For example, increased amounts of a given enzyme may be produced to meet the demands of a new environmental condition.
The tendency to produce a single phenotype even under changing conditions.
A subgroup of a population that is locally adapted, that differs genetically and phenotypically from the main population, but is not reproductively isolated from it.
Epigenetic system
Series of properties emerging from the interaction among genes.
Fine grained variation
Environmental changes that affect organisms during their lifetime. As opposed to coarse grained variation or changes in the environment that are produced at intervals longer than the life span of an individual.
Form (or morph)
Phenotypic variant that arises as a result of an interaction with the environment (ecomorph).
Gene regulation
A mechanism of phenotypic plasticity by which genes of an individual are turned on and off, frequently producing conspicuous phenotypic alterations.
Heteroblastic development
The production of several forms throughout the existence of an individual. As opposed to plasticity, in heteroblastic development the changes from one form to another are already programmed in the genes of the organism. Such forms will be expressed at some point in the life of the individual regardless of environmental change.
Modular organism
An individual composed of repeated anatomical units (e.g., internodes in plants), and with the capability of growing continuously throughout its life.
Form. Note that this is but one of the morphologies which can appear in one genotype. A term without common use in one specific way, nevertheless widely utilized.
Parallel evolution
The process by which distantly related taxa develop a similar phenotypic appearance because natural selection acted in similar ways upon them.
Phenotypic plasticity
The capability of a single genotype to produce several physiological and morphological phenotypes under changing environmental conditions. It is the result of a modification in the activity of expressed genes (see allelic sensitivity) or a rearrangement of the information contained in the genotype (see gene regulation). Phenotypic plasticity is a broader term that embraces acclimation, chromatic adaptation, heterophylly due to plasticity, etc.
Genetic and/or phenotypic variation within a single population. In the recent literature (and in the present paper), this term most commonly refers to genetic variability.
Reaction norm
Set of potential phenotypes that a genotype can produce when it thrives in a changing environment.
Although there is a great debate and there are different concepts of species (e.g., biological, morphological, ecological, phylogenetic, etc.) available from the literature, we have used the biological species concept throughout the paper. That is, a cohesive group of reproductively compatible individuals.
Subgroup within a population, that may be locally adapted (ecotype), but still maintains reproductive ties with the rest of the genotypes in the metapopulation (the species as a whole). The designation of a variety should have a genetic basis.


We thank Dr. R. Moe and an anonymous reviewer for various valuable suggestions which added to the clarity of this presentation. Additionally we acknowledge numerous other friends and colleagues, both here and abroad, for their suggestions, comments and criticisms over time as this text developed; our viewpoint concerning the role of the environment was certainly enriched. It is our hope that this paper will serve as a starting point for the more frequent gathering of, and utilization of, data relating to plastic responses, as we continue to probe the realities in the natural world.


An, S., Friedl, T., and Hegewald, E. 1999.
Phylogenetic relationships of Scenedesmus and Scenedesmus-like coccoid green algae as inferred from ITS-2 rDNA sequence comparisons. Plant Biology 1: 418–428.
Arber, A. 1919.
On heterophylly in water plants. American Naturalist 53: 272–278.
Arber, A. 1972.
Water Plants. A study of Aquatic Angiosperms. 436 pp. J. Cramer, New York.
Armstrong, S.L. 1997.
The behavior in flow of the morphologically variable seaweed Hedophyllum sessile (C. Ag.) Setchell. Hydrobiologia 183: 115–122.
Baldwin, J.M. 1896.
A new factor in evolution. American Naturalist 30:441–451; 536–553.
Barker, H.A. 1935.
Photosynthesis in diatoms. Archiv für Mikrobiologie 6: 141–156.
Baurain, D., Renquin, L., Grubisic, S., Scheldeman, P., Belay, A., and Wilmotte, A. 2002.
Remarkable conservation of internally transcribed spacer sequences of Arthrospira (“Spirulina”) (Cyanophyceae, Cyanobacteria) strains from four continents and of recent and 30-year-old dried samples from Africa. Journal of Phycology 38: 234–393.
Beijerinck, M. 1890.
Cultuversuche mit Zoochlorellen, Lichenengonidien und anderen niederen Algen. Botanische Zeitung 48: 725–739.
Bell, G. 1991.
The ecology and genetics of fitness in Chlamydomonas III. Genotype-by-environment interaction within strains. Evolution 45: 668–679.
Bell, G. 1992.
The ecology and genetics of fitness in Chlamydomonas. V. The relationship between genetic correlation and environmental variance. Evolution 46: 561–566.
Ben-Amotz, A. 1975.
Adaptation of the unicellular alga Dunaliella parva to a saline environment. Journal of Phycology 11: 50–54.
Blanchette, C.A. 1997.
Size and survival of the intertidal plants in response to wave action: a case study with Fucus gardneri. Ecology 78: 1563–1578.
Borowitzka, M.A. and Volcani, B.E. 1978.
The polymorphic diatom Phaeodactylum tricornutum: Ultrastructure of its morphotypes. Journal of Phycology 14: 10–21.
Bradshaw, A.D. 1965.
Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics 13: 115–155.
Campbell, E.O. and Sarafis, V. 1972.
Schizomeris---growth form of Stigeoclonium tenue (Chlorophyta: Chaetophoraceae). Journal of Phycology 8: 276–282.
Chabot, B. and Chabot, J. 1977.
Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26: 363–377.
Chodat, R. and Malinesko, O. 1893.
Sur le polymorphisme de Scenedesmus acutus Meyen. Bulletin de l'Herbier Boissier 1: 184–190.
Clack, T., Mathews, S., and Sharrock, R.A. 1994.
The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Molecular Biology 25: 413–427.
Clausen, J., Keck, D., and Hiesey, W.M. 1940.
Experimental Studies on the Nature of Plant Species. I. Effect of Varied Environment on Western North American Plants. Carnegie Institution of Washington, Washington, DC.
Cocke, E.C. 1967.
The Myxophyceae of North Carolina. Edwards Brothers, Inc., North Carolina. 206 pp.
Cook, C.D.K. 1968.
Phenotypic plasticity with particular reference to three amphibious plant species. In Heywood, V. (ed.), Modern Methods in Plant Taxonomy. Pp. 97–111. Academic Press, London.
Cook, S.A. and Johnson, M.P. 1968.
Adaptation to heterogeneous environments. I. Variation in heterophylly in Ranunculus flammula L. Evolution 22: 496–516.
Cox, E.J. 1995.
Morphological variation in widely distributed diatom taxa: taxonomic and ecological implications. In Marino, D. and Montresor, M. (eds.) Proceedings of the 13th International Diatom Symposium 1994. Pp. 335–345. Biopress, Bristol.
Cox, E.J. 1996.
Identification of Freshwater Diatoms from Live Material. Chapman & Hall, London, UK. 158 pp.
Darley, W.M. 1968.
Deoxyribonucleic acid content of the three cell types of Phaeodactylum tricornutum Bohlin. Journal of Phycology 4: 219–220.
Darwin, C. 1859.
On the origin of species. Watts & Co. London, U.K. 426 pp.
Dawes, C.J., Moon, R., and La Claire, J. 1976.
Photosynthetic responses of the red alga, Hypnea musciformis (Wulfen) Lamouroux (Gigartinales). Bulletin of Marine Science 26: 467–473.
de Jong, G. 1995.
Phenotypic plasticity as a product of selection in a variable environment. American Naturalist 145: 493–512.
Desikachary, T.V. 1959.
Cyanophyta. Indian Council of Agricultural Research Monographs on Algae. Times of India Press, Bombay, India. 686 p.
DeWitt, T.J. 1998.
Costs and limits of phenotypic plasticity: tests with predator-induced morphology and life history in a freshwater snail. Journal of Evolutionary Biology 11: 465–480.
DeWitt, T.J., Sih, A., and Wilson, D.S. 1998.
Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution 13: 77–81
Drouet, F. and Daily, W.A. 1956.
Revision of coccoid Myxophyceae. Butler University Botanical Studies 12: 1–218.
Fain, S.R. and Murray, S.N. 1982.
Effects of light and temperature on net photosynthesis and dark respiration on gametophytes and embryonic sporophytes of Macrocystis pyrifera. Journal of Phycology 18: 92–98.
Foerster, J.W. 1964.
The use of calcium and magnesium hardness ions to stimulate sheath formation in Oscillatoria limosa (Roth) C.A. Agardh. Transactions of the American Microscopical Society 83: 420–427.
Francke, J.A. and ten Cate, H.J. 1980.
Ecotypic differentiation in response to nutritional factors in the algal genus Stigeoclonium Kütz. (Chlorophyceae). British Phycological Journal 15: 343–355.
Francke, J.A. and Simons J. 1984.
Morphology and systematics of Stigeoclonium Kütz. (Chaetophorales). In Irvine, D.E.G. and John, D.M. (eds.). Systematics of the Green Algae. Pp. 363–377. Academic Press, New York.
Gause, G.F. 1947.
Problems of evolution. Transactions of the Connecticut Academy of Arts and Sciences 37: 17–68.
Geitler, L. 1932.
Cyanophyceae. In Rabenhorst, L. (ed.). Kryptogamen-Flora von Deutschland, Österreich und der Schweiz 14: 673–1056.
Geitler, L. 1968.
Kleinsippen bei Diatomeen. Österreichische Botanische Zeitschrift 115: 354–362.
Goldschmidt, R.B. 1940.
The Material Basis of Evolution. Yale University Press, New Haven, Connecticut. 436 pp.
Gomez, N., Riera, J.L., and Sabater, S. 1995.
Ecology and morphological variability of Aulacoseira granulata (Bacillariophyceae) in Spanish reservoirs. Journal of Ultrastructural Research 17: 1–16.
Gomulkiewicz, R. and Kirkpatrick, M. 1992.
Quantitative genetics and the evolution of reaction norms. Evolution 46: 390–411.
Graham, L.E. and Wilcox, L.W. 2000.
Algae. Prentice-Hall. Upper Saddle River, New Jersey. USA. 640 pp.
Grintzesco, J. 1902.
Reserches expérimenteles sur la morphologie et la physiologie de Scenedesmus acutus Meyen. Bulletin de l'Herbier Boissier 2: 217–264.
Grunow, A. 1859.
Die Desmidiaceen und Pediastreen einiger Österreichischen Moore, nebst einigen Bemerkungen über beide Familien im Allgemeinen. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 8(Abh.): 489–502.
Gutenbrunner, S.A., Thalhamer, J., and Schmid, A.M. 1994.
Proteinaceous and immunochemical distinctions between the oval and fusiform morphotypes of Phaeodactylum tricornutum (Bacillariophyceae). Journal of Phycology 30: 129–136.
Håkansson, H. and Chepurnov, V. 1999.
A study of variation in valve morphology of the diatom Cyclotella meneghiniana in monoclonal cultures: effect of auxospore formation and different salinity conditions. Diatom Research 14: 251–272.
Havel, J.E. 1987.
Predator-induced defenses: a review. In Kerfoot, W.C. and Sih, A. (Eds.), Predation: Direct and Indirect Impacts on Aquatic Communities. Pp. 263–278. University Press of New England. Hanover, New Hampshire.
Hegewald, E.H. 1997.
Taxonomy and phylogeny of Scenedesmus. Algae 12: 235–246.
Hegewald, E. 2000.
New combinations in the genus Desmodesmus (Chlorophyceae, Scenedesmaceae). Archiv für Hydrobiologie Supplement 131: 118.
Hegewald, E.H. and Silva, P. 1988.
An annotated catalogue of Scenedesmus and nomenclaturally related genera including original descriptions and figures. Bibliotheca Phycologica 80: 1–587.
Huxley, J.S. 1942.
Evolution, The Modern Synthesis. Allen and Unwin, London. 645 pp.
Jeeji-Bai, N. 1977.
Morphological variation of some species of Calothrix and Fortiea. Archiv für Protistenkunde 119: 367–387.
Jeeji-Bai, N. and Seshadri, C.V. 1980.
On coiling and uncoiling of trichomes in the genus Spirulina. Archiv für Hydrobiologie Supplement 60: 32–47.
Johannsen, W. 1911.
The genotype conception of heredity. American Naturalist 45:129–159.
Kaplan, D.R. 1980.
Heteroblastic leaf development in Acacia: Morphological and morphogenetic implications. Cellule 73: 137–203.
Kehoe, D.M. and Grossman, A.R. 1996.
Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273: 1409–1412.
Krammer, K. and Lange-Bertalot, H. 1991.
Bacillariophyceae. 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. In Ettl, H., Gerloff, J., Gärtner, G., Heynig, H., and Mollenhauer, D. (eds.) Süsswasserflora von Mitteleuropa Vol. 2(3): 1–576. Gustav Fisher Verlag, Germany.
Ku, S. and Hunt, L. 1973.
Effects of temperature on the morphology and photosynthetic activity of newly matured leaves of alfalfa. Canadian Journal of Botany 51: 1907–1916.
Lazaroff, N. 1966.
Photoinduction and photoreversal of the nostocacean developmental cycle. Journal of Phycology 2: 7–17.
Lazaroff, N. and Vishniac, W. 1961.
The effect of light on the developmental cycle of Nostoc muscorum, a filamentous blue-green alga. Journal of General Microbiology 25: 365–374.
Lazaroff, N. and Vishniac, W. 1964.
The relationship of cellular differentiation to colonial morphogenesis of the blue-green alga, Nostoc muscorum A. Journal of General Microbiology 35: 447–457.
Levin, D.A. 1988.
Plasticity, canalization and evolutionary stasis in plants. In Davy, A.J., Hutchings, M.J., and Watkinson, A.R. (eds.) Plant Population Ecology. Pp. 35–45. The 28th Symposium of the British Ecological Society, Sussex, 1987. Blackwell Scientific Publications, England.
Levins, R. 1968.
Evolution in Changing Environments. Princeton University Press, N.J. 120 pp.
Lewin, J.C., Lewin, R.A., and Philpott, D.E. 1958.
Observations on Phaeodactylum tricornutum. Journal of General Microbiology 18: 418–426.
Livingston, B. 1900.
On the nature of the stimulus which causes the change in form in polymorphic green algae. Botanical Gazette 30: 289–417.
Lürling, M. 1999.
The Smell of Water. Grazer-induced colony formation in Scenedesmus. Wageningen Agricultural University. The Netherlands. 270 pp.
MacArthur, R. and Levins, R. 1967.
The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101: 377–387.
Mann, D.G. 1989.
The species concept in diatoms: evidence for morphologically distinct sympatric gamodemes in four epipelic species. Plant Systematics and Evolution 164: 215–237.
Mann, D.G. 1999.
The species concept in diatoms. Phycologia 38: 437–495.
Mathieson, A.C. and Burns, R.L. 1971.
Ecological studies of economic red algae. I. Photosynthesis and respiration of Chondrus crispus Stackhouse and Gigartina stellata (Stackhouse) Batters. Journal of Experimental Marine Biology and Ecology 7: 197–206.
Mayr, E. and Provine, W.E. (eds.). 1980.
The Evolutionary Synthesis: Perspectives on the Unification of Biology. Harvard University Press, Cambridge, Massachusetts. 487 pp.
Mazel, D. and Marliere, P. 1989.
Adaptive eradication of methionine and cysteine from cyanobacterial light-harvesting proteins. Nature 341: 245–248.
Morales, E.A. 2001.
Morphological studies in selected fragilarioid diatoms (Bacillariophyceae) from Connecticut waters, USA. Proceedings of the Academy of Natural Sciences of Philadelphia 151: 39–54.
Morales, E.A. and Trainor, F.R. 1997.
Algal phenotypic plasticity: its importance in developing new concepts. The case for Scenedesmus. Algae 12: 147–157.
Morales, E.A. and Trainor, F.R. 1999.
Phenotypic plasticity in Scenedesmus: implications for algal taxonomy and ecology. Gayana, Botánica 56: 77–86.
Norton, T.A., Mathieson, A.C., and Neushul, M. 1981.
Morphology and Environment. In Lobban, C.S. and Wynne, M.J. The Biology of Seaweeds. pp. 421–451. University of California Press. Los Angeles, CA.
Ogata, E. 1966.
Photosynthesis in Porphyra tenera and some other marine algae as affected by Tris(hydroxymethyl)-aminomethane in artificial media. Botanical Magazine of Tokyo 79: 271–282.
Pigliucci, M. 1996.
How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). Trends in Ecology and Evolution 11: 168–173.
Pigliucci, M. 2001.
Phenotypic Plasticity. Beyond Nature and Nurture. The Johns Hopkins University Press. Baltimore, USA. 328 pp.
Pigliucci, M., Schlichting, C.D., Jones, C.S., and Schwenk, K. 1996.
Developmental reaction norms: Interactions among allometry, ontogeny and plasticity. Plant Species Biology 11: 69–85.
Pringsheim, E.G. 1968.
Phycology in the field and in the laboratory. Journal of Phycology 3: 93–95.
Reimann, B.E.F. and Volcani, B.E. 1968.
Studies on the biochemistry and fine structure of silica shell formation in diatoms. III. The structure on the cell wall of Phaeodactylum tricornutum Bohlin. Journal of Ultrastructural Research 21: 182–193.
Robinson, B.L. and Miller, J.H. 1970.
Photomorphogenesis in the blue-green alga Nostoc commune 584. Physiologia Plantarum 23: 461–472.
Round, F. 1996.
Fine detail of siliceous components of diatom cells. Beihefte zur Nova Hedwigia 112: 201–213.
Round, F. 1997.
Genera, species and varieties - are problems real or imagined? Diatom 13: 25–29.
Rumrich, U., Lange-Bertalot, H., and Rumrich, M. 2000.
Diatomeen der Anden. Von Venezuela bis Patagonien/Feuerland Und Zwei weitere Beiträge. Iconographia Diatomologica 9: 1–673.
Santelices, B. 1978.
The morphological variation of Pterocladia caerulescens (Gelidiales, Rhodophyta) in Hawaii. Phycologia 17: 53–59.
Schaal, B.A. and Leverich, W.J. 1987.
Genetic constraints on plant adaptive evolution. In Loeschcke, V. (ed.), Genetic Constraints on Adaptive Plant Evolution. Pp. 173–184. Sprinter-Verlag, Berlin.
Scheiner, S.M. 1993.
Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24: 35–68.
Scheiner, S.M. 1998.
The genetics of phenotypic plasticity. VII. Evolution in a spatially-structured environment. Journal of Evolutionary Biology 11: 303–320.
Scheiner, S.M. and Lyman, R.F. 1989.
The genetics of phenotypic plasticity. I. Heritability. Journal of Evolutionary Biology 2: 95–107.
Schlichting, C.D. 1986.
The evolution of phenotypic plasticity in plants. Annual Review of Ecology and Systematics 17: 667–693.
Schlichting, C.D. 1989.
Phenotypic integration and environmental change. BioScience 39: 460–464.
Schlichting, C.D. and Pigliucci, M. 1993.
Control of phenotypic plasticity via regulatory genes. American Naturalist 142: 366–370.
Schlichting, C.D. and Pigliucci, M. 1995.
Gene regulation, quantitative genetics and the evolution of reaction norms. Evolutionary Ecology 9: 154–168.
Schlichting, C.D. and Pigliucci, M. 1998.
Phenotypic Evolution: A Reaction Norm Perspective. Sinauer Associates, Sunderland, MA. 387 p.
Schlichting, H.E. and Bruton, B.A. 1970.
Some problems of pleomorphism in algal taxonomy. Lloydia 33: 472–476.
Schmalhausen, I. 1949.
Factors of Evolution: The Theory of Stabilizing Selection. Blakiston, Philadelphia, Pennsylvania.
Schmid, A.M.M. 1997.
Intraclonal variation of the tripolar pennate diatom “Centronella reicheltii” in culture: strategies for reversion to the bipolar Fragilaria-form. Nova Hedwigia 65: 27–45.
Schultz, M.E. 1971.
Salinity-related polymorphism in the brackish-water diatom Cyclotella cryptica. Canadian Journal of Botany 49: 1285–1289.
Senn, G. 1899.
Ueber einige Koloniebildende einzellige Algen. Botanische Zeitung 57:39–104.
Shubert, L.E. 1975.
Scenedesmus trainorii sp. nov. (Chlorophyta, Chlorococcales): a polymorphic species. Phycologia 14: 177–182.
Sinclair, C. and Whitton, B.A. 1977.
Influence of nitrogen source on morphology of Rivulariaceae (Cyanophyta). Journal of Phycology 13: 335–340.
Smith, G.M. 1916.
A monograph of the algal genus Scenedesmus based upon pure culture studies. Transactions of the Wisconsin Academy of Science, Arts and Letters 18: 422–530.
Sorokin, C. and Krauss, R.W. 1962.
Effects of temperature and illuminance on Chlorella growth uncoupled from cell division. Plant Physiology 37: 37–42.
Stam, W.T. and Holleman, H.C. 1975.
The influence of different salinities on growth and morphological variability of a number of Phormidium strains (Cyanophyceae) in culture. Acta Botanica Neerlandica 24: 379–390.
Stearns, S.C. 1982.
The role of development in the evolution of life histories. In Bonner, J. (ed.), Evolution and Development. Pp. 237–258. Springer-Verlag, New York.
Stearns, S.C. 1989.
The evolutionary significance of phenotypic plasticity. BioScience 39:436–445.
Stein, J.R. 1963.
Morphological variation in Tolypothrix in culture. British Phycological Bulletin 2: 206–210.
Sultan, S.E. 1987.
Evolutionary implications of phenotypic plasticity in plants. Evolutionary Biology 21: 127–178.
Theriot, E. 1987.
Principal components analysis and taxonomic interpretation of environmentally related variation in silicification of Stephanodiscus (Bacillariophyceae). British Phycological Journal 22: 359–373.
Trainor, F.R. 1998.
Scenedesmus: phenotypic plasticity. Beihefte zur Nova Hedwigia 117: 1–367.
Trainor, F.R. and Hilton, R.L. 1963.
Culture of Scenedesmus longus. Bulletin of the Torrey Botanical Club 90: 407–12.
Trainor, F.R. and Morales, E.A. 1999.
Recent trends in the taxonomy of selected chlorococcalean algae. In Vidyavati and Mahato, A.K. (eds.) Recent trends in algal taxonomy. Vol. 1: Taxonomical Issues. Vedams, New Delhi, India.
Trainor, F.R., Rowland, H, Lylis, J., Winter, P., and Bonanomi, P. 1971.
Some examples of polymorphism in algae. Phycologia 10: 113–19.
Turesson, G. 1922.
The genotypical response of the plant species to the habitat. Hereditas 3: 211–350.
Via, S. 1993.
Adaptive phenotypic plasticity: target or by product of selection in a variable environment. American Naturalist 142: 352–365.
Via, S., Gomulkiewicz, R., de Jong, G., Scheiner, S.M., Schlichting, C.D., and van Tienderen, P.H. 1995.
Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology and Evolution 10: 212–217.
Via, S. and Lande, R. 1985.
Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39: 505–522.
Waaland, S.D. and Cleland, R. 1972.
Development in the red alga, Griffithsia pacifica: control by internal and external factors. Planta 105: 196–204.
Waddington, C.H. 1942.
Canalization of development and the inheritance of acquired characters. Nature 150: 563–565.
Weismann, A. 1885.
Die Kontinuität des Keimplasmas als Grundlage einer Theorie der Verenbung. Gustav Fisher, Jena, Germany.
Wilde, A., Churin, Y., Schubert, H., and Börner, T. 1997.
Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. Federation of European Biological Societies Letters 406: 89–92.
Winn, A. 1996.
Adaptation to fine-grained environmental variation: An analysis of within-individual leaf variation in an annual plant. Evolution 50: 1111–1118.
Whitlock, M.C. 1996.
The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. American Naturalist 148: S65-S77.
Wolle, F. 1887.
Fresh-water algae of the United States. The Comenius Press. Bethlehem, Pennsylvania. 364 p.
Woltereck, R. 1909.
Weiterer experimentelle Untersuchungen über Artveränderung, speziell über das Wesen Quantitativer Artunterschiede bei Daphniden. Verhandlungen der Deutsche Zoologische Gesellschaft 19: 110–172.
Wright, S. 1931.
Evolution in Mendelian populations. Genetics 16: 97–159.
Wright, S. 1932.
The roles of mutation, inbreeding, crossbreeding, and selection in evolution. Proceedings of the Sixth International Congress of Genetics 1: 356–366.
Yarish, C., Edwards, P., and Casey, S. 1979.
A culture study of salinity responses in ecotypes of two estuarine red algae. Journal of Phycology 15: 341–346.
Yeh, C.-C., Wu, S.-H., Murphy, J.T., and Lagarias, J.C. 1997.
A cyanobacterial phytochrome two-component light sensory system. Science 277: 1505–1508.
Young, J., Dickinson, T., and Dengler, N. 1995.
A morphometric analysis of heterophyllous leaf development in Ranunculus flabellaris. International Journal of Plant Sciences 156: 590–602.
Zirbel, M.J., Veron, F., and Latz, M.I. 2000.
The reversible effect of flow on the morphology of Ceratocorys horrida (Peridinales, Dinophyta). Journal of Phycology 36: 46–58.

Tables and Figures

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Table 1. As we recognize the fact that a number of older Scenedesmus/Desmodesmus species protologues (approximately 330) were not descriptions of discrete taxa but merely of a developmental stage, the number of taxa (or species) is initially reduced; we have used the example of a cake to symbolize this concept (Fig. 3). However, with additional interpretations, the species number does not necessarily remain low. As we learn to utilize additional stable characters, and eventually molecular information, over time numbers of well defined species might increase, even markedly! We could consider cutting a separate cake with both thick and thin slices. Thick slices characterize species with even more genotypes, while a thin slice would represent a species with fewer genotypes. The latter would possess a more restricted variability for plasticity, and no doubt be ecologically less successful.
Initially, an abundance of taxa. 330
With recognition of an ordered developmental sequence, based solely on morphological features, the number of taxa decreases. The organisms could be displayed in a layered cake; 20 slices equal 20 species.
Over time, with more data, the species number slowly increases, with light microscopy level morphological similarity coupled with SEM differences. Much, much thinner slices of the cake. 70
Some morphologically similar thin slices are revealed to be physiologically different, i.e., some of these 70 (above) species are polyphyletic. We can no longer use the slice of the layered cake example. 200
Two isolates, with identical morphs, differ in the duration of display of each morph. . 250
Transitions between individual morphs is more gradual with considerable overlap. 300
Combinations of two or more of the above characters, coupled with DNA sequence data. 400