Mollusks are interesting to both collectors and scientists for a number reasons, not the least of which is that speciation within many mollusk families can be remarkably extensive. We assume that there has been selection in favor of each, based on Darwinian fitness assumptions, but the picture is a bit more complex than it may at first appear. Genetics, particularly in the 1920s-1940s attempted to explain species change solely in terms of loss or replacement ot specific genes thought to control a phenotype, whether this control involved gene operating cooperatively or singly. Darwin was, of course, unaware of genetics. Current research highlights some unanswered questions within the genetic, or neo-Darwinian, explanation for phenotype development and expression.
First, a point that Darwin himself complained about, is that observable characteristics are impermanent. Not only do these traits change, but there is no definite number of traits (morphologic or genetic) that differentiate one taxonomic species from another.
Second, as every developmental biologist knows, the maternal and/or external environment surrounding an embryo or neonate can have a profound effect on the adult phenotype and this effect may appear heritable
Observations of phenotype plasticity in response to varying environment are not new (Baldwin, 1902: Vermeij, 1969 Waddington,1975), and neither are the related observations of phenotype switching (Minton & Gundersun, 2001: West-Eberhardt, 2003. p. 108). Darwin did say that species will change over time in response to environmental conditions. He also noted that use or disuse of body parts led to changes over time.
Over the ensuing decades, phenoplasticity has been extensively researched. The developmental emergence of phenotype is currently believed to be based on epigenetic control mechanisms. These mechanisms explain how environmental or tissue factors silence or modify DNA (Schlicting & Pigliucci, 1998). Differences are not to be found in the DNA structure, itself, but rather in a plethora of internal and external factors: microRNAs protein fragments, hormones, etc (Pray, 2004). A molecular mode for signaling pathways has recently been worked out as well, in this case for emergence of the adult form of the nematode, Caenorhabditis elegans (Ambros, 2003).
Phenotype plasticity is a common feature of many species It is found across a wide range of phyla, including vertebrate invertebrate, plant, and algal species, and it is most frequently expressed in early developmental stages of the organism. It is specific response of individuals, not populations, to a change in the physical and/or biological environment, and it involves some signaling pathway. What this amounts to is that a phenotype may indeed be proposed by the organism's genetic structure, but it will be determined by the interaction between an individual's genes and exogenous (tissue or environmental) factors outside the developing fertilized cell.
At the extreme, the ultimate effect of an environmental factor on an individuals genotype may be to completely change the phenotype of the individual. If the environmental factor continues to operate, the progeny of that individual will express the new phenotype, but will, in fact, switch or revert to the unchanged phenotype should the environment revert (Schlicting & Pigliucci. 1998). Several specific criteria should he considered when assessing a presumptive phenoplastie response:
- The phenotype has a heritable basis, which can be transmitted to and expressed in the progeny.
- A signaling pathway is triggered externally.
- The changed phenotype is usually revertible to the ancestral or unchanged phenotype when external conditions revert.
A study of the South African beach clam, Donax serra (Röding, 1798) (Fig. 1) showed phenoplasticity for shape and shell density: i.e.. a heritable capability responding to particular environmental cues (Soares et al., 1998). Phenoplastic switching may also underlie the numerous color morphs of this clam species. In this ease, the clam occupies a fine-grained, high energy habitat, conditions that may favor a phenoplastic response
Fig. 1 . Donax serra (Röding, 1798) from South Africa. These two specimens are approximately 52 mm and represent two different forms or color morphs that may be habitat caused. On the left is Donax serra (f. aurantiaca Krauss, 1848) from tidal areas near fresh water (considered a subspecies by some authors). On the right is Donax serra serra, from marine tidal areas.
One of the more interesting molluscan studies involved the snails Physa gyrina Say, 1821, and P. acuta Draparnaud. 1805 (studied as the synonym P. heterostropha Say, 1817)( Fig. 2). These calcium-limited freshwater snails lack sufficient calcium to simultaneously strengthen the shell by making it thicker and narrow the aperture by adding special structures like barricading teeth. The developmental dilemma is: 1) to make a wide aperture and invest more in making a robust shell, thus leaving the snail vulnerable to crayfish predators: or 2) to make a narrow aperture with barricades and a thinner shell, thus leaving the snail vulnerable to fish that can crush the shell. DeWitt (1995, 1998) showed that natural populations of these two snails, where crayfish were the primary predators, had a higher frequency of the narrow aperture elongate shells; those more exposed to fish predator had the stronger more rotund, wide-aperture shells. The clincher was when P. gyrina and P. acuta were each reared for a month in water containing either crayfish or fish, a significant fraction facultatively modified their morphology to defend selectively against the predator present. The phenoplasticity of the family Physidae has resulted in a plethora of named forms. According to Dillon et al. (2005), rather than the 40 named species that were until recently attributed to this family, there are in fact only about 10 distinct species.
Fig. 2. The two shells on the left are Physa gyrina Say. 1821 (17-20mm) and the two on the right are Physa acuta Draparnaud, 1805 (14-15mm). In both species the smaller shell on the right shows some thickening of the shell around the aperture. Most literature still refers to Physa acuta as the synonymous Physa heterostropha Say, 1817. These sinistral or left-handed pond snails are wide-ranging throughout much of the United States and are difficult to properly identify.
Phenoplasticity is also common among the living species of the genus Crepidula and leads to high variability and much taxonomic confusion (Fig. 3). The substrate on which the snail grows affects its shell shape, leading to environmental responses that become further exaggerated owing to accomodation among correlated traits (Hoagland, 1979).
Fig. 3 Various species of Crepidula, all of which vary in shape depending upon the substrate. The species illustrated vary in size from 19 to 32mm. a. Crepidula aculeata (Gmelin, 1791); b. C. convexa Say, 1822; c. C. costata Sowerby, 1824; d. C. glauca Say, 1822; e. C. fornicata (Linnaeus, 1758); f. C. lessonii Broderip, 1834; g. C. piano Say, 1822; h. C. porcellana (Linnaeus, 1758); i. C. onyx Sowerby, 1824. The variability of Crepidula species has caused and continues to cause taxonomic problems.
Finally there are some interesting examples of phenoplasticity in the family Neritidae. In Hawaii, the endemic Neritona granosa (G. B. Sowerby I, 1825) (Fig. 4) varies in shell structure between the typical pustulose surface found in specimens from downstream locations and a much smoother shell in upstream locations. This gradient between tough and smooth forms is usually correlated with altitude, with waterfalls and their associated plunge pools serving as abrupt boundaries between these ecotypes (Ford, 1987). Vermeij (1969) speculated that the rough surface broke up the lamellar flow of fast currents over the shell, helping the animal retain its grip on the substrate. Way et al. (1993) demonstrated that there was no difference to the force applied to a pustulose or a smooth shell. The fact remains, however, that the shell structure differs, most likely due to an as yet undetermined habitat cue.
Fig. 4. Neritona granosa (Sowerby, 1825) (18-35mm) from fast flowing freshwater streams in the Hawaiian Islands. The two lower specimens demonstrate the variability in shell structure. The shell on the left is from the upper reaches of the stream where the shells are typically smooth and the shell on the right is from the lower reaches where the shells have the rough surface normally associated with this species
The well-known zebra nerite of the Caribbean, Puperita pupa (Linnaeus, 1767), is found among intertidal rocks as a small white shell with black zebra-like stripes (Fig. 5). The same species found in nearby spring-fed "essentially fresh water" pools is a black shell with white spots. This freshwater form was named as a distinct species, Puperita tristis (Orbigny, 1842). Gunderson and Minton (1997, 2001) found what they thought were intermediate forms of Puperita pupa living in freshwater pools alongside the black form with white spots. They transplanted some normal Puperita pupa (black stripes on white) from saltwater to freshwater pools and some P. tristis forms (white spots on black) from freshwater into saltwater pools. The freshwater pools actually measured 8.7ppt (dissolved salts in parts per thousand) which is by formal definition actually considered brackish. The salt water pools measured approximately 37.4ppt. Three months later they observed the transplanted P. pupa forms had begun laying down shell that was black with white spots and the transplanted P. tristis forms had begun laying down normal P. pupa black stripes on a white shell. Both cases are a reversal of the original shell pattern and probably indicate a single species with a phenoplastic response to salinity.
Fig. 5 The small (7mm) Caribbean nerite Puperita pupa (Linnaeus, 1767) has both a marine variant (top row, left two shells) and a "freshwater" variant (top row, right two shells). If moved from one habitat to another, the shell pattern changes. Bottom row left shows a change of pattern from marine to fresh water, while bottom row right shows a pattern change of fresh water to marine. §
Mollusks may prove to be good candidates for further phenoplasticity studies. Both genetically inherited traits and phenoplastic response may determine an organism's morphology. Further study and some simple experimentation will help unravel and delineate these processes.
Ambros, Victor. 2003. "MicroRNA pathways in flies and worms: growth. death, fat, stress and timing," Cell 113, pp. 673-676,
Baldwin, J. M. 1902. Development and Evolution, MacMillan, NY.
Dewitt, T. J. 1995. "Functional Tradeoffs and Phenotypic Plasticity in the Freshwater Snail, Physa," Ph.D. dissertation. Binghampton University (SUNY).
Dewitt, T. J. 1998. "Costs and limits of phenotypic plasticity: tests with predator induced morphology and life history in a freshwater snail.'' J. Evolutionary Biology 11. pp. 465-480.
Dillon, R.T., Jr.; Wethington, A.R.; Rhett, J.M; and Smith, T.P. 2002. "Populations of the European freshwater pu1monate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra, Invertebrate Biology 121(3). pp. 226-234.
Ford, J. I. 1987. 'Biology, microhabitat and intraspecific shell variation of Neritina granosa Sowerby (Prosobranchia Neritidae) in Hawaiian streams." Bulletin of Marine Science 41(2). p 635.
Gunderson, Ross and Minton, Russell. 1997. "Do spots equal stripes?" American Conchologist 25(4), pp. 22-23.
Hoagland, K. E. 1979. "Systematic review of fossil and recent Crepidula and discussion of evolution of the Calyptraeidae," Malacologia 16. pp. 353-420.
Minton, Russell L. and Gunderson, Ross W. 2001. "Puperita tristis (d'Orhigny. 1842) (Gastropoda: Neritidae) is an ecotype of Puperita pupa (Linnaeus, 1767),'' American Malacological Bul. 16(1/2). pp. 13-20.
Pray, Leslie A. 2004. "Epigenetics: Genome, Meet Your Environment:" The Scientist 18(13). July 5, 2004, pp. 14-23.
Schlicting, Carl D. and Pigliucci, Massimo. 1998. Phenotypic Evolution: A Reaction Norm Perspective, Sinauer Associates, Inc., MA.
Snares, A., Callahan, R.IC, and De Ruyck, A.M.C. 1998. "Microevolution and phenotypic plasticity in Donax serra Röding (Bivalvia: Donacidae) on high energy sandy beaches," J. Molluscan Studies 64. Oxford University Press, pp. 407 421.
Vermeij, Geerat J. 1969 ''Observations on the shells of some freshwater neritid gastropods from Hawaii and Guam.'' Micronesica 51(1) 155-162
Waddington, C. H. 1975. Evolution of an Evolutionist, Cornell University Press. p. 219.
Way, Carl N. I., Burky, Albert J.; and Lee, Michael T. 1993. "The relationship between shell morphology and microhabitat flow in the endemic Hawaiian stream limpet (Hihiwai), Neritina granosa (Prosobranehia: Neritidae)." Pacific Science 47(3). pp. 263-275
West-Eberhardt, Mary Jane. 2003. Developmental Plasticity, Oxford University Press, pp. 34-35.
- Genotype. The genetic coding for properties of structure and function in an organism.
- Phenoplasticity. The ability of an organism to alter properties of structure and function in differing environments while retaining the original genotype.
- Phenotype. The observable properties of structure and function of an organism as determined by its genetic makeup and modified by its reaction to the environment (i.e.. what an organism looks like).
* Burton E. Vaughan, Adjunct Professor of Biological Sciences, Washington State University-Tricities, http://shells.tricity.wsu.edu, firstname.lastname@example.org
† Thomas E. Eichhorst, 4528 Quartz Dr., NE Rio Rancho, NM 87121-1908, email@example.com
§ The research by Gunderson and Minton into the color morphs of Puperita pupa was first reported in American Conchologist. December 1997, Vol. 25(4) and was funded by a COA grant.