Burky, Albert J.

Guttman, S. I.

Hornbach, Daniel J.

McLeod, M. J.

Way, C. M.

English

University of Dayton

University of DaytoneCommonsBiology Faculty Publications Department of Biology1981Environmental Heterogeneity, Genetic-Polymorphism, and Reproductive StrategiesM. J. McLeodDaniel J. HornbachS. I. GuttmanC. M. WayAlbert J. BurkyUniversity of Dayton, aburky1@udayton.eduFollow this and additional works at: https://ecommons.udayton.edu/bio_fac_pubPart of the Biology CommonsThis Response or Comment is brought to you for free and open access by the Department of Biology at eCommons. It has been accepted for inclusionin Biology Faculty Publications by an authorized administrator of eCommons. For more information, please contact frice1@udayton.edu,mschlangen1@udayton.edu.eCommons CitationMcLeod, M. J.; Hornbach, Daniel J.; Guttman, S. I.; Way, C. M.; and Burky, Albert J., "Environmental Heterogeneity, Genetic-Polymorphism, and Reproductive Strategies" (1981). Biology Faculty Publications. 18.https://ecommons.udayton.edu/bio_fac_pub/18NOTES AND COMMENTS 129 ENVIRONMENTAL HETEROGENEITY, GENETIC POLYMORPHISM, AND REPRODUCTIVE STRATEGIES The debate over the relationship between intrapopulation genetic variation and the degree of environmental heterogeneity is an enduring one (Valentine 1976; Templeton 1977; Powell and Wistrand 1978; Vrijenhoek 1978, 1979; Spieth 1979). Levins (1968), in a theoretical presentation, suggested that genetic variability would be higher in an unstable environment han in one that was more homogene- ous. The hypothesis was that genetic variability would be required to accommo- date variation in the environment. Modifications of this hypothesis have been presented as data on the genetics of populations has accumulated. For example, a great deal of variability has been found in populations of deep sea invertebrates (Ayala et al. 1974, 1975), where one would expect a relatively stable environment and hence, little intrapopulation variation. To account for the high variation, a relationship was suggested between trophic resource stability and population genetic variability that would allow specialists to subdivide the resource. Genic variation in populations has also been related to the size and mobility of the organisms; large, motile animals would pass over many microhabitats and would adapt as generalists (Selander and Kaufman 1973). Rigorous proof of a positive correlation between environmental heterogeneity and intrapopulation genetic variation is, however, still lacking. This is largely because of the difficulty of identifying and measuring variant environmental parameters, and the lack of comparisons of nonspecific populations. In addition, the relationship between environmental variability and reproduc- tive strategies has received much attention. Classically, reproductive strategies have been interpreted in relation to r- and K-selection theory, which predicts that in stable environments the best strategy is to produce few young with high energy content (K-strategy) while the opposite strategy (r-strategy) would be optimum in a more variable environment. Recently, however, many examples have been given which do not conform to the classical r- and K-selection theory. Other theories to account for these variations have been published and are reviewed by Stearns (1976, 1977) and Calow (1973). Giesel (1976) indicates that little attention has been paid to the relationship between reproductive strategies and genetic variability. For primarily inbreeding species, classical theory suggests a simple, highly structured genetic makeup. Each population consists of a number of inbred, monomorphic lines with most of the heterozygotes being found in the occasional hybrids between different monomorphic lines (Allard 1970; Hutchinson 1965). Experimental support for this theory has recently been found in both plants and animals (Rick and Fobes 1975; Selander and Hudson 1976). This report provides data on the relationship between environmental heterogeneity, genetic poly- morphism, and reproductive strategies, for the freshwater clam Musculium partumeium. Am. Nat. 1981. Vol. 118, pp. 129-134. ? 1981 by The University of Chicago. 0003-0147/81/1801-0064$02.00 This content downloaded  on Fri, 18 Jan 2013 18:20:10 PMAll use subject to JSTOR Terms and Conditions130 THE AMERICAN NATURALIST TABLE 1 ALLELIC FREQUENCIES FOR EACH POLYMORPHIC LOCUS IN Two POPULATIONS OF Musculium partumeium Locus Allele DW AM PEP-3 .................... a .26 ... b .72 1.00 C .02 ... PEP-4 .................... a .31 b .66 1.00 C .03 ... EST-8 .................... b .77 1.00 C .23 ... PGI-1 .................... d .98 1.00 e .02 ... PGI-3 .................... b .45 c .55 1.00 Sphaeriid clams (including the genus Musculium) are ovoviviparous and simul- taneous hermaphrodites. It is known that these clams are capable of self- fertilization (Thomas 1959; Heard 1965) but the degree to which self-fertilization occurs in nature is not known. Self-fertilization potentially permits a single indi- vidual to establish a new population after passive dispersal by waterfowl and/or aquatic insects (Rees 1965; Mackie 1979). However, dispersal mechanisms provide a potential means of genetic input to the population on a continuing basis. Recently, in a study of the related genus Sphaerium, inbreeding with occasional outcrossing was suggested as the major mode of reproduction (Hornbach et al. 1980a). Individuals of Musculium partumeium were collected from two locations in west-central Ohio. The first site was an ephemeral pond located on a virgin stand woodlot (Drew Woods=DW). The second site was a permanent (remaining full on a seasonal basis) pond formed approximately 20 yr ago by damming a stream which drained a marsh (Aullwood Marsh=AM). Care was taken to collect indi- viduals from a large area at each site to minimize the possibility of sampling a single genetic cohort. Standard techniques of horizontal starch gel electrophoresis and histochemical staining were employed (Selander et al. 1971; Ayala et al. 1972). Ten enzyme systems (isocitrate dehydrogenase, phosphoglucomutase, acid phosphatase, xanthine dehydrogenase, glutamate oxaloacetate transaminase, catalase, peptidase (PEP), phosphoglucose isomerase (PGI), esterase (EST), and nonspecific protein) encoding 22 presumptive genetic loci were consistently re- solved. If several forms of the same enzyme were present and each was controlled by a separate gene locus, a hyphenated numeral was added to the abbreviation for the enzyme. The enzyme with the greatest anodal migration was called 1, the next 2, and so on. When allelic variation occurred, the allele with the greatest anodal migration was called a, the next b, and so on. Five loci (Pep-3, Pep-4, Est-8, Pgi-I, Pgi-3) were polymorphic in samples from the ephemeral pond. The collec- tion from the permanent pond, however, was completely monomorphic at every locus. The allelic frequencies at each of the polymorphic loci are given in table 1. This content downloaded  on Fri, 18 Jan 2013 18:20:10 PMAll use subject to JSTOR Terms and ConditionsNOTES AND COMMENTS 131 TABLE 2 GENETIC VARIATION IN Two POPULATIONS OF Musculijun DW AM .. ............. 49 45 % heterozygosity ... ......... 6.14 0 % polymorphism* ... ......... 18.18 0 % polymorphism .... ........ 22.72 0 * Mean percentage of loci polymorphic per population where the most common allele has a frequency of .95 or less. t Mean percentage of loci polymorphic per population where the most common allele has a frequency of .99 or less. Percent heterozygosity (table 2) suggests that there is some outbreeding in the ephemeral site, although this is limited in its occurrence. Nei's (1972) standard genetic distance (an estimate of the number of electrophoretically detectable codon differences per locus) between the two populations is 0.0198. In terms of the genetic structure of the two populations, the population from the ephemeral habitat is much more variable than the one from the permanent pond. Passive dispersal is undoubtedly a mechanism for genetic input into both ponds (Rees 1965; Mackie 1979). However, gene frequencies are probably not due to passive input, but instead the result of environmental pressures. Further, the percentage of polymorphic loci and heterozygosity indicate that several genetic lines exist in the ephemeral population. The low amount of heterozygosity, how- ever, suggests that self-fertilization or inbreeding within lines is the rule and that outbreeding between lines occurs only rarely. This idea is further supported by the fact that genotypic frequencies for only one polymorphic locus (Pgi-1) are in Hardy-Weinberg equilibrium. That this one locus is in equilibrium is most easily explained as a chance event. To relate the genetic data to reproductive strategies it is necessary to outline briefly the life histories of the two populations (see Hornbach et al. 1980b; and Way et al. 1980 for a more complete description). The ephemeral pond (DW: pond surface area 1,042 M2; maximum depth 0.9 m) usually has a single generation per year. Young are born in the spring and early summer (May-July), remain dormant as juveniles in the dry substrate (August-January), begin growth in March, repro- duce, and then die when the pond dries in late summer. The permanent pond (AM: pond surface area 396 M2; maximum depth 0.7 m) has two generations per year. The first generation is born between May and July (AM-SG). These individuals grow during August and September and then give birth between September and November. Some adults of the spring generation overwinter and contribute to the next spring generation. Young of the fall genera- tion (AM-FG) overwinter as subadults and experience rapid growth and repro- duction in the spring. Most of the fall generation die by the end of July, but some survive to contribute to the new fall generation. Life-history parameters for these populations (from Hornbach et al. 1980b; Way et al. 1980; unpublished data) indicate that they do not support r- and K-se- This content downloaded  on Fri, 18 Jan 2013 18:20:10 PMAll use subject to JSTOR Terms and Conditions132 THE AMERICAN NATURALIST lection theory. The annual selection ratio (no. of young born per average adult) for the ephemeral pond, DW (25: 1), is lower than for either generation from the permanent pond, AM (38: 1 and 136: 1 for AM-FG and AM-SG, respectively); however the energy content for newborns from DW (37.03 ,ugC) is greater than for newborns from AM (21.82 and 24.21 ,ugC for AM-FG and AM-SG, respectively). The intrinsic rate of increase (r) for DW (0.0084 day-1) is lower than for AM (0.0115 day-1 and 0.0304 day-1 for AM-FG and AM-SG, respectively). In terms of productivity, the turnover time (time needed for the population to produce the average standing crop biomass) for DW (73 days) is greater than for AM (36 and 61 days for AM-FG and AM-SG, respectively) indicating that productivity is lowest in the temporary pond (DW). Two theories deal specifically with the effect of environmental stability on the evolution of life-history traits. One theory (a deter- ministic theory) proposes that populations inhabiting stable environments tend to have low intrinsic rates of increase, with few young of high energy content (K-strategy), whereas those populations which inhabit more variable environ- ments tend to have higher intrinsic rates of increase, with more young of lower energy content (r-strategy). The other theory (a stochastic theory) holds that when juvenile mortality fluctuates more than adult mortality, the combination of life- history traits expected with the deterministic theory (r- and K-selection) will be reversed. The stochastic theory (not r- and K-selection) probably applies to the populations of M. partumeium at AM and DW. In the ephemeral pond, mortality for adults is probably less variable than for juveniles since the majority of adults die over a relatively short period of time (several weeks) as the pond dries, while juvenile mortality extends over many months. Thus, the ephemeral nature of the pond at DW probably results in mortality varying more for juveniles than adults and could reverse the reproductive tactic predicted by r- and K-selection theory. These findings support a bet-hedging strategy put forth by Steams (1976, 1977) rather than r- and K-selection theory. It would seem obvious, then, that the population in the ephemeral pond is adapted to its habitat on several levels. Genetically, the population supports a high amount of variability (relative to the AM population). This presumably allows the population to remain adapted to the harsh conditions and also possibly subdivide the habitat so that different monomorphic genetic lines become, in effect, spe- cialists. Reproductively, the population opts for quality over quantity. By en- dowing the young with a high energy content, they are prepared to endure a harsh winter in a dry pond. It appears that this adaptation is, at least partly, on a phenotypic level. This is suggested by the fact that in the odd year when the pond at Drew Woods does not dry, a second generation can be produced in the fall. This pattern is like that for the population in the permanent pond (AM). However, only 19% of the spring-born clams at DW grew in late summer to produce the second generation in the fall of 1979 when the pond remained full. The population from the permanent pond has exploited its environment by taking the opposite tactic. This population has introduced a highly productive second generation each year and has spread out the available reproductive energy to many young. Also, in view of the potential of continued genetic input through passive dispersal, the monomorphism exhibited by this population indicates that This content downloaded  on Fri, 18 Jan 2013 18:20:10 PMAll use subject to JSTOR Terms and ConditionsNOTES AND COMMENTS 133 the genetic composition has been streamlined by selection; the reproductive strategy of self-fertilization helps to maintain this genetic uniformity. ACKNOWLEDGMENT This work was supported by the Miami University Faculty Research Commit- tee. LITERATURE CITED Allard, R. W. 1970. Population structure and sampling methods. Pages 97-107 in 0. H. Frankel and E. Bennett, eds. Genetic resources in plants-their exploration and conservation. Davis, Philadelphia. Ayala, F. J., J. B. Powell, M. L. Tracey, C. A. Mourdo, and S. Perez-Salas. 1972. Enzyme variability in the Drosophila willistoni group. IV. Genic variation in natural populations of Drosophila willistoni. Genetics 70:113-139. Ayala, F. J., J. W. Valentine, L. B. Barr, and G. S. Zumwalt. 1974. Genetic variability in a temperate intertidal phoronid, Phoronopsis viridis. Biochem. Genet. 11:413-427. Ayala, F. J., J. W. Valentine, D. Hedgecock, and L. B. Barr. 1975. Deep-sea asteroids: high genetic variability in a stable environment. Evolution 29:203-212. Calow, P. 1973. The relationship between fecundity, phenology, and longevity: a systems approach. Am. Nat. 107:559-574. Giesel, J. T. 1976. Reproductive strategies as adaptations to life in temporally heterogeneous environ- ments. Annu. Rev. Ecol. Syst. 7:57-79. Heard, W. H. 1965. Comparative life histories of North American pill clams (Sphaeriidae: Pisidium). Malacologia 2:381-411. Hombach, D. J., M. J. McLeod, S. I. Guttman, and S. K. Seilkop. 1980a. Genetic and morphological variation in the freshwater clam, Sphaerium (Bivalvia: Sphaeriidae). J. Molluscan Stud. 46: 158-170. Hombach, D. J., C. M. Way, and A. J. Burky. 1980b. Reproductive strategies in the freshwater sphaeriid clam, Musculium partumeium (Say), from a permanent and a temporary pond. Oecologia (Berl.) 44:164-170. Hutchinson, J. B. 1965. Crop plant evolution: a general discussion. Pages 166-181 in J. B. Hutchinson ed. Essays on crop plant evolution. Cambridge University Press, Cambridge. Levins, R. 1968. Evolution in changing environments. Princeton University Press, Princeton, N.J. Mackie, G. L. 1979. Dispersal mechanisms in Sphaeriidae (Mollusca: Bivalvia). Bull. Am. Malacol. Union. 45:17-21. Nei, M. 1972. Genetic distance between populations. Am. Nat. 106:283-292. Powell, J. R., and H. Wistrand. 1978. The effect of heterogeneous environments and a competitor on genetic variation in Drosophila. Am. Nat. 112:935-948. Rees, W. J. 1965. The aerial dispersal of Mollusca. Proc. Malacol. Soc. Lond. 36:269-282. Rick, C. M., and J. F. Fobes. 1975. Allozymes of Galapagos tomatoes: polymorphism, geographic distribution, and affinities. Evolution 29:443-457. Selander, R. K., and R. 0. Hudson. 1976. Animal population structure under close inbreeding: the land snail Rumina in southern France. Am. Nat. 110:695-718. Selander, R. K., and D. W. Kaufman. 1973. Genic variability and strategies of adaptation in animals. Proc. Natl. Acad. Sci. USA 70:1875-1877. Selander, R. K., M. H. Smith, S. Y. Yang, W. E. Johnson, and J. B. Gentry. 1971. Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse (Peromnyscus polionotus). Univ. Texas Publ. 7103:49-90. Spieth, P. T. 1979. Environmental heterogeneity: a problem of contradictory selection pressures, gene flow, and local polymorphism. Am. Nat. 113:247-260. Stearns, S. C. 1976. Life-history tactics: a review of the ideas. Q. Rev. Biol. 51:3-47. This content downloaded  on Fri, 18 Jan 2013 18:20:10 PMAll use subject to JSTOR Terms and Conditions134 THE AMERICAN NATURALIST . 1977. The evolution of life-history traits: a critique of the theory and a review of the data. Annu. Rev. Ecol. Syst. 8:145-171. Templeton, A. R. 1977. Survival probabilities of mutant alleles in fine-grained environments. Am. Nat. 111:951-966. Thomas, G. J. 1959. Self-fertilization and production of young in a sphaeriid clam. Nautilus 72:131- 140. Valentine, J. W. 1976. Genetic strategies of adaptation. Pages 78-94 ill F. J. Ayala, ed. Molecular evolution. Sinauer, Sunderland, Mass. Vrijenhoek, R. C. 1978. Coexistence of clones in heterogeneous environments. Science 199:549-552. . 1979. Genetics of a sexually reproducing fish in a highly fluctuating environment. Am. Nat. 113:17-29. Way, C. M., D. J. Hornbach, and A. J. Burky. 1980. Comparative life history tactics of the sphaeriid clam, Musculium parturneium (Say), from a permanent and a temporary pond. Am. Midl. Nat. 104:319-327. M. J. MCLEOD BIOLOGY DEPARTMENT BELMONT ABBEY COLLEGE BELMONT, NORTH CAROLINA 28012 D. J. HORNBACH* S. I. GUTTMAN C. M. WAY ZOOLOGY DEPARTMENT MIAMI UNIVERSITY OXFORD, OHIO 45056 A. J. BURKY BIOLOGY DEPARTMENT UNIVERSITY OF DAYTON DAYTON, OHIO 45469 Submitted July 30, 1979; Revised June 23, 1980; Accepted November 7, 1980 * Present address: Department of Biology, University of Virginia, Charlottesville, Virginia, 22901 This content downloaded  on Fri, 18 Jan 2013 18:20:10 PMAll use subject to JSTOR Terms and Conditions

Environmental Heterogeneity, Genetic-Polymorphism, and Reproductive Strategies

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Environmental Heterogeneity, Genetic-Polymorphism, and Reproductive Strategies

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