Phenotypic plasticity and the maintenance of genetic variation.
Protracted selection for intermediate optima should deplete the additive genetic (heritable) variance of polygenic traits (Via and Lande 1985 and references therein). Nevertheless, much heritable variation is retained in quantitative skeletal characters in a broad range of living organisms, including those with static morphologies (Cheverud 1982; Cheetham et al. 1993). One plausible explanation is that polygenic mutation rates may be sufficiently high to balance the effects of selection (Lande 1976; Via and Lande 1985, 1987; Lynch 1988, 1990). However, attention is increasingly turning to the ability of a genotype to produce different phenotypes in response to environmental cues (phenotypic plasticity) as a possible alternative (Gillespie and Turelli 1989; Stearns 1992; Scheiner 1993).
To shield a trait from genetic depletion, plasticity must itself include a genetic component, the genotype-by-environment (G x E) interaction, resulting from differences among genotypes in the amount and form (reaction norm) of response to environmental cues (Via and Lande 1985, 1987; Gillespie and Turelli 1989). Thus, the phenotypic ranks of genotypes and their fitness can vary among environments, so that no one genotype is superior in all environments. Expressed as a proportion of the phenotypic variance of a trait, the G x E interaction is a measure of the heritable component of plasticity, analogous to heritability of the trait itself (Scheiner and Lyman 1989).
Quantitative-genetic models differ in regarding plasticity either as a trait in its own right, controlled by genes separate from those that determine trait means (Scheiner and Lyman 1989; Gavrilets and Scheiner 1993a,b), or as a function of the differential expression of the same gene in different environments (Via and Lande 1985, 1987; Via 1987). The models are not mutually exclusive, and their implications for the effectiveness of plasticity in maintaining genetic variation are still controversial (Gillespie and Turelli 1989, 1990; Gimelfarb 1990; Zhivotovsky and Gavrilets 1992; Scheiner 1993). Empirical data supporting each model are reviewed by Scheiner (1993).
Much evidence has been found for the heritability of plasticity, particularly in plants, insects, and mice (reviewed by Scheiner 1993). Data are lacking, however, for taxa with detailed fossil records, especially those showing static species morphologies. The cheilostome bryozoan Stylopoma is one such taxon (Cheetham and Jackson 1995). Breeding experiments on two living species of Stylopoma have shown that significant levels of heritable genetic variation are preserved in quantitative traits of skeletal morphology, despite the long-term stabilizing selection to which these species were apparently subjected (Cheetham et al. 1993; Cheetham and Jackson 1995). Thus, Stylopoma is an especially appropriate taxon in which to investigate the possible evolutionary role of phenotypic plasticity.
Bryozoa grow as colonies of phenotypically variable modules termed zooids. Zooids within a colony are clone mates. The morphologic differences among ordinary feeding zooids at the same stage of development in a colony are termed "microenvironmental" variation, on the assumption that they represent response of a single genotype to environmental cues varying on small spatial and temporal scales during growth of the colony (Boardman and Cheetham 1969; Boardman et al. 1970, 1983). To the extent that differences between zooids within colonies cannot be associated with known environmental cues, this usage is consistent with the more general application of "microenvironmental" to "variation below the resolution of the experimental method or beyond the control of the experimenter" (Scheiner et al. 1991). Such variation is difficult to separate from differences caused by random errors of development uncorrelated with environmental cues ("developmental noise") (Bull 1987; Via 1987, 1993; Scheiner et al. 1991).
By the usual definition, phenotypic plasticity is limited to variation associated with discrete differences in environmental conditions (Bradshaw 1965; Bull 1987; Via 1987, 1993). Only by association with discrete environmental cues can the shapes of reaction norms for genotypes be determined and compared. For bryozoans, differences in environments are usually observable on spatial scales exceeding the size of a single colony and thus are termed "macroenvironmental" (Hughes 1992). Nevertheless, experimental evidence suggests that variation within bryozoan colonies can represent response to environmental cues and thus reflect reaction norms. Changes in zooid morphology within cheilostome colonies have been induced by varying temperature, food supply, or the presence and absence of predators (Menon 1972; Jebram 1978; Harvell 1984, 1986). However, the heritability of such environmental response has not been investigated for traits of zooid morphology. Hughes (1992) has shown that life-history traits (colony growth rates) in the cheilostome Celleporella include a G x E interaction by growing pieces of colonies under different conditions of water flow during different seasons of the year.
Without experimental manipulation, the environmental component of among-colonies phenotypic variation is difficult to separate from differences caused by genotype. Within-colony variation averages 50%-70% of the total phenotypic variance in traits of skeletal morphology in a variety of cheilostome species collected from a variety of habitats (Jackson and Cheetham 1990; Cheetham et al. 1993, 1994). Thus, only 30%-50% remains on average for genetic and environmental among-colonies variance combined. The same appears to be true for life-history traits. When the experimental design includes pieces of the same colony (clone mates) grown under the same conditions only a few centimeters apart, within-colony variation accounts for 70% of the variance in colony growth rates (Hughes 1992).
In Stylopoma, heritable genetic variation in the skeletal morphology of parental colonies collected from a variety of habitats averages 34% of total phenotypic variance, leaving little apparent room for environmental differences among colonies from either the same or different habitats (Cheetham et al. 1993). However, the relationships among these components of variance in zooid morphology have not been evaluated in detail.
In this paper, we explore the potential for phenotypic plasticity to preserve genetic diversity in two species of Stylopoma whose skeletal morphology has remained static for 8 my or more. With breeding data on living populations of these species, we estimate: (1) environmental and genetic components of the phenotypic variation in ten traits of zooid skeletal morphology, and (2) the heritability of within-colony environmental variability in each trait as a possible vehicle for preserving genetic variation.
MATERIALS AND METHODS
The common-garden experiment of our previous studies of the inheritance of species identities and the heritability and genetic covariance of traits of skeletal morphology in two species of Stylopoma provided the data for this analysis (Jackson and Cheetham 1990; Cheetham et al. 1993). Offspring of maternal colonies collected from local populations at seven sites averaging 25 km apart (range, 4-64 km) over 110 km of the Caribbean coast of Panama from Portobelo to the Holandes Cays (Herrera et al. 1995) were raised at a common site at the San Blas station of the Smithsonian Tropical Research Institute. Thirty-eight maternal colonies of species 1 from seven sites produced 111 offspring in which at least three zooids in the same stage of development could be measured; 44 colonies of species 2 from five sites yielded 215 such offspring. Paternity in all cases is unknown. The numbers of maternal colonies per collection site vary from 1 to 21 (mean, 5.43; geometric mean, 3.14) in species 1 and 1 to 30 (mean, 14.67; geometric mean, 6.48) in species 2. Offspring per parent vary from 1 to 11 (mean, 2.92; geometric mean 2.23) in species 1 and 1 to 18 (mean, 4.89; geometric mean, 3.35) in species 2. The ten traits of skeletal morphology (table 1) employed here are the ones previously used to distinguish the species morphometrically and establish the inheritance of their identities (Jackson and Cheetham 1990).
Imbalance in the numbers of colonies among sites and within families and the limited sizes of offspring colonies complicate the analysis. Measurement of three zooids per colony in these species produces relatively stable colony means, with standard errors averaging only 6.5%-7.8% (table 1). However, colony variances are much more unstable, with standard errors averaging 80.8%-83.6% (table 1). By doubling the sample size to six zooids in the parental colonies, we were able to reduce the instability of their variances by approximately half. It was not possible to measure more zooids at the same stage of development in most of the offspring, but offspring values are averaged for each parent in calculating heritabilities, in effect reducing instability by a comparable amount.
To evaluate the genetic and environmental components of phenotypic variation in each species, we partitioned the phenotypic variance in each trait by separate nested ANOVAs on parents and offspring. The levels of variation in each ANOVA are: among sites from which maternal colonies were collected (SITES), among colonies within sites (COLONIES), and among zooids within colonies (ZOOIDS). In addition [TABULAR DATA FOR TABLE 1 OMITTED] to the usual hierarchical tests of significance between the levels of variation (Sokal and Rohlf 1969), we estimated the added variances associated with each level. These estimates were calculated from the appropriate mean squares and proportional cell frequencies, to avoid problems of nonadditivity because of the unbalanced design (Winer 1971).
Parental and offspring ANOVAs should yield similar but not identical estimates of phenotypic variance at the two lower levels (ZOOIDS and COLONIES). If within-colony variation represents response to environmental cues, the ZOOIDS-level variance of parents should be greater than that of offspring, because the common environment in which the offspring colonies were grown was much less variable spatially and temporally than the sites at which parents were collected. Collection sites for the most part represent different reefs with different, seasonally varying exposure to sediment, water flow, and other factors. Within each site, the variety of environments from which colonies were collected (on pinnacles and in channels, and with different biotic associations) is even greater than the overall differences between reefs. The COLONIES-level variances for both parents and offspring include estimates of the genotypic variation within sites, but parental variances should also include a greater environmental component reflecting this heterogeneity in the natural reef environment. However, this environmental effect could be counteracted by an increased genotypic diversity for offspring relative to parents, reflecting the (unknown) paternal contribution.
At the highest level in the ANOVAs (SITES), variances for the parents and offspring could be quite different. Parental variances should include both environmental and genetic variation reflecting the differences (or simply the distances) between sites, whereas those for the offspring should be virtually entirely genetic because of their growth in the common garden. We took advantage of this difference to obtain estimates of environmental and genetic components of the phenotypic variance among sites.
To evaluate the G x E interaction in each trait, we estimated the heritability of within-colony variability as though plasticity is a trait itself (Scheiner and Lyman 1989), using the data for parents and offspring combined. The alternative approach of estimating the genetic correlation between the phenotypic expressions of a trait for each genotype in two or more environments (Via and Lande 1985, 1987; Via 1993) is not possible for these bryozoans because the conditions inducing changes in zooid morphology within colonies are unknown.
For each colony, plasticity was calculated as the variance among zooids divided by the total phenotypic variance of the generation (parent or offspring) to which the colony belongs. Heritability of plasticity was based on offspring mean, parental value regressions weighted for unequal family size (Falconer 1963, 1981). The weights previously obtained for the regressions using trait values (Cheetham et al. 1993) were used for these calculations. We emphasize that our use of this method of estimating the G x E component of environmental variance in these species is a practical expedient, and is not intended to imply a belief that plasticity is controlled by genes separate from those determining the trait means.
Components of Phenotypic Variation
The distribution of phenotypic variance components is remarkably similar for the two species of Stylopoma, despite striking numerical differences in some of the variances (e.g., FPD in tables 2 and 3) and the strong imbalance in sampling design. In both species, phenotypic variance is concentrated at the two lower levels, zooids within colonies (ZOOIDS) and colonies within sites (COLONIES), for both parents and offspring (tables 4 and 5). The two levels together account for 89%-91% of the variance in species 1 and 96%-97% in species 2, averaged across traits.
Variation among zooids within colonies (ZOOIDS) averages 55%-67% of phenotypic variance in species 1 (table 4) and 63%-76% in species 2 (table 5), accounting for more than 40% of the variance in every trait. Within-colony variances are higher for parents than offspring in seven of ten [TABULAR DATA FOR TABLE 2 OMITTED] cases in species 1 and eight of ten in species 2 (compare ZOOIDS columns of parents vs. offspring in tables 2 and 3). This difference is consistent with the greater variability of environments at the sites from which parents were collected relative to the common environment in which offspring were grown. The difference amounts to 12%-13% of the phenotypic variance on average for both species (means of parents vs. offspring in zooids in colonies columns; tables 4, 5).
Variance among colonies within sites (COLONIES) is smaller than that within colonies (ZOOIDS) in all cases but LO in species 1 (compare COLONIES versus ZOOIDS columns for parents and offspring; tables 2, 3). On average, the COLONIES component accounts for 24%-34% of total phenotypic variation in species 1 and 21%-33% in species 2 (means in colonies in sites columns, tables 4 and 5), about half as much as within-colony variation. Nevertheless, the added effect of among-colonies variance is significant at P [less than] 0.001 in 32 of 40 cases, and nonsignificant (P [greater than] 0.05) in only two (LAV for both parents and offspring in species 1) (tables 2, 3). COLONIES-level variances are higher for offspring than parents in nine of ten cases in each species (tables 2, 3), suggesting that any effects of environmental heterogeneity within sites are more than balanced by increased genotypic diversity of offspring resulting from the unknown [TABULAR DATA FOR TABLE 3 OMITTED] paternal contribution. Thus, variance among colonies within sites appears to reflect genetic variation little diluted by environmental effects.
In contrast, there is little evidence for important contributions to either genotypic or environmental variance at the highest level, colonies among different sites (SITES) (tables 2, 3). Two traits in each species show significant or marginally significant SITES components, but the traits are different between species (WO and LS, orificial characters, in species 1; LAV and OAV, avicularian characters, in species 2). Moreover, seven of ten among-sites variances (including the two significant at P [less than] 0.10) are greater among parent colonies in species 1, and thus probably environmental, but four of ten (including the two significant at P [less than] 0.10 and P [less than] 0.001) are greater among offspring colonies in species 2, and thus probably genetic. Together, the among-sites genetic and environmental components average only 9.2% of phenotypic variance in species 1 and 3.4% in species 2 (tables 4, 5).
Heritability of within-Colony Variability
Table 6 shows heritabilities of within-colony variabilities (environmental, ZOOIDS-level variance) for the two species of Stylopoma, compared with heritabilities of the trait means. [TABULAR DATA FOR TABLE 4 OMITTED] The latter are approximately the same as the COLONIES-level variance components, thus confirming that almost all of the phenotypic variation in zooid morphology among colonies within sites is additive genetic, not environmental.
Significant heritability for variability is apparent in 9 of 20 cases compared to 13 of 20 for the traits (table 6). On average, the heritable components of trait variability are lower in both species than those of the traits themselves. Moreover, unlike the trait heritabilities, these components differ in average value between species. There is little correspondence between trait and variability heritabilities in magnitude or significance in either species. However, the significance of these differences is obscured by the greater sampling instability of within-colony variances compared to within-colony means (table 1). The heritabilities of variability for two traits in each species (WZ and LO in species 1; LZ and LAV in species 2) are significant at P [less than] 0.01 or less (table 6), making it highly likely that the environmental component of phenotypic variation in these species includes a G x E interaction.
Phenotypic variance in zooidal skeletal morphology appears to be virtually a two-component system in Stylopoma, comprising environmental variation within colonies and additive genetic variation among colonies in local populations (within sites). The scant evidence for phenotypic variation among sites, either environmental or genetic, is unexpected, given the sessile mode of life and limited ability for larval dispersal of cheilostomes such as Stylopoma (Jackson 1986). However, these results are consistent with the low levels of genetic difference between populations based on data from protein electrophoresis (Jackson and Cheetham 1990). For Stylopoma species 2, Nei's unbiased distances among the five sites analyzed here average 0.021 (range 0.000-0.047, SE = 0.006), well within the values (mean 0.031, SE = 0.007) for genetically little-differentiated, freely interbreeding local populations in the extensively sampled Drosophila willistoni group of species (Ayala 1983). (Data are insufficient to calculate genetic distances for the seven populations of Stylopoma [TABULAR DATA FOR TABLE 5 OMITTED] species 1.) Nei's unbiased distance between the two species of Stylopoma is 1.11 (Jackson and Cheetham 1990), which compares closely with the average of 1.056 for non-sibling species of the D. willistoni group (Ayala 1983).
Within-colony variability is maintained at a level averaging two-thirds of phenotypic variance in both the markedly heterogeneous environments of the collection sites and the more uniform conditions of the common garden. However, it is higher in the natural reef environments, suggesting a relationship to discrete environmental cues, and thus to reaction norms rather than random "developmental noise." Random variability is commonly linked to low levels of heterozygosity (Palmer and Strobeck 1986 and references therein), but evidence from protein electrophoresis suggests that the level of heterozygosity in cheilostomes, including Stylopoma, is as high as in typical outbreeding organisms (Jackson and Cheetham 1990). Although standard gel electrophoresis overestimates heterozygosity (Leigh Brown and Langley 1979), there is no reason to suspect that the results for Stylopoma should be different from those for other organisms. Thus, cheilostome within-colony variability appears to represent genuine phenotypic plasticity, comparable with that experimentally induced by discrete environmental cues, including life history traits (Hughes 1992).
The nearly 2:1 ratio between environmental variance (within-colony variability) and genetic differences in trait means is modified by significant G x E interaction, providing a possible mechanism for preserving the genetic diversity of traits and the potential basis for evolution of plasticity. Averaged across traits, the heritabilities of plasticity in Stylopoma are 34%-69% of those of the traits (table 6), typical of the proportions found in a wide variety of organisms and types of traits (Scheiner 1993). The heritability of plasticity is a more elusive property than that of the traits because of the large sampling errors associated with estimating variances (table 1). Indeed, Hughes (1992) found environmental changes in the phenotypic ranks of genotypes for colony growth rates in spite of an absence of statistically significant G x E interaction. In this perspective, the evidence for heritability of plasticity in Stylopoma is all the more convincing.
[TABULAR DATA FOR TABLE 6 OMITTED]
All of these relationships suggest that heritable plasticity could be a basis for maintaining genetic diversity in cheilostomes. It is important to note that the amount of plasticity itself appears to have been maintained at a nearly constant level of 50%-70% of phenotypic variance, averaged across traits, for millions of years (Cheetham et al. 1994), perhaps under the same forces of stabilizing selection as the traits. This may justify regarding cheilostome plasticity as a trait, rather than as a byproduct of evolution of trait means.
It is also possible that genetic diversity is maintained in cheilostomes simply by a balance between mutation and selection. Rates of phenotypic differentiation between Stylopoma species are consistent with random change (Cheetham et al. 1993; Cheetham and Jackson 1995), assuming mutation rates typical for polygenic traits in a wide range of organisms (Lynch 1988, 1990). However, mutation rates for cheilostome morphologic traits are unknown, and the balance hypothesis would explain these results only if plasticity is a trait subject to the same forces of selection and rates of mutation.
The presence of heritable variation in phenotypic plasticity alters response to directional selection (Gavrilets and Scheiner 1993b; Scheiner 1993). Thus, the high levels of selective mortality calculated for divergence of Stylopoma species by directional selection (Cheetham et al. 1993) may need to be reconsidered. Selection intensities could be either higher or lower than those calculated, depending on the correlations among shape coefficients of the reaction norms (Gavrilets and Scheiner 1993b; Scheiner 1993). More experiments associating zooid phenotypes with discrete environmental cues are needed to determine reaction norms. The sensitivity of plasticity to environmental heterogeneity in Stylopoma should make experimentation possible.
We thank J. Sanner and A. Herrera for technical assistance, C. D. Harvell and an anonymous reviewer for helpful comments on the manuscript, and the Kuna Nation and the Government of Panama for permitting work in the San Blas. This work was supported by the Smithsonian Scholarly Studies Program, the Marie Bohrn Abbott Fund of the National Museum of Natural History, and the Smithsonian Tropical Research Institute.
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ALAN H. CHEETHAM Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560
JEREMY B. C. JACKSON Center for Tropical Paleoecology and Archaeology, Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama
LEE-ANN C. HAYEK Statistics and Mathematics, Smithsonian Institution, Washington, D.C. 20560
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|Title Annotation:||Quantitative Genetics of Bryozoan Phenotypic Evolution, Part 3|
|Author:||Cheetham, Alan H.; Jackson, Jeremy B.C.; Hayek, Lee-Ann C.|
|Date:||Apr 1, 1995|
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