Population size and identity influence the reaction norm of the rare,endemic plant Cochlearia bavarica across a gradient of environmental stress

Habitat degradation and loss can result in population decline and genetic erosion, limiting the ability of organisms to cope with environmental change, whether this is through evolutionary genetic response (requiring genetic variation) or through phenotypic plasticity (i.e., the ability of a given genotype to express a variable phenotype across environments). Here we address the question whether plants from small populations are less plastic or more susceptible to environmental stress than plants from large populations. We collected seed families from small (<100) versus large natural populations (>1,000 flowering plants) of the rare, endemic plant Cochlearia bavarica (Brassicaceae). We exposed the seedlings to a range of environments, created by manipulating water supply and light intensity in a 2 x 2 factorial design in the greenhouse. We monitored plant growth and survival for 300 days. Significant effects of offspring environment on offspring characters demonstrated that there is phenotypic plasticity in the responses to environmental stress in this species. Significant effects of population size group, but mainly of population identity within the population size groups, and of maternal plant identity within populations indicated variation due to genetic (plus potentially maternal) variation for offspring traits. The environment x maternal plant identity interaction was rarely significant, providing little evidence for genetically- (plus potentially maternally-) based variation in plasticity within populations. However, significant environment x population-size-group and environment x population-identity interactions suggested that populations differed in the amount of plasticity, the mean amount being smaller in small populations than in large populations. Whereas on day 210 the differences between small and large populations were largest in the environment in which plants grew biggest (i.e., under benign conditions), on day 270 the difference was largest in stressful environments. These results show that population size and population identity can affect growth and survival differently across environmental stress gradients. Moreover, these effects can themselves be modified by time-dependent variation in the interaction between plants and their environment.     

Genetic architecture and maternal contributions of early‐life survival in lake trout Salvelinus namaycush

The influences of additive, non‐additive and maternal effects on early survival (uneyed embryo survival, eyed embryo survival, alevin survival and overall survival to first feeding) were quantified in lake trout Salvelinus namaycush using a 7 × 7 full‐factorial breeding design. Maternal effects followed by non‐additive genetic effects explained around one third of the phenotypic variance of the survival traits. Although the amount of additive genetic effects were low (<1%), suggesting a limited potential of the traits to respond to new selection pressures, how maternal and non‐additive genetic effects may respond to selection under certain circumstances are discussed.     

Quantitative genetic analysis of larval life history traits in two alpine populations of Rana temporaria

We estimated genetic and maternal variance components of larval life history characters in alpine populations of Rana temporaria (the common frog) using a full-sib/half-sib breeding design. We studied trait plasticity by raising tadpoles at 14 or 20°C in the laboratory. Larval period and metamorphic mass were greater at 14°C. Larval period did not differ between populations, but high elevation metamorphs were larger than low elevation metamorphs. Significant additive variation for larval period was detected in the low altitude population. No significant additive variation was detected for mass at metamorphosis (MM), which instead displayed significant maternal effects. Plasticity in metamorphic mass of froglets was greater in the high altitude population. The plastic response of larval period to temperature did not differ between the populations. Evolution of metamorphic mass is likely constrained by lack of additive genetic variation. In contrast, significant heritability for larval period suggests this trait may evolve in response to environmental change. These results differ from other studies on R. temporaria, suggesting that populations of this broadly distributed species present substantial geographic variation in the genetic architecture and plasticity of tadpole life history traits.     

Patterns of genetic variation in desiccation tolerance in embryos of the terrestrial-breeding frog, pseudophryne guentheri

Environmental change often requires evolutionary responses, and therefore understanding the genetic architecture of susceptible populations is essential for predicting their capacity to respond adaptively. However, quantitative genetic studies are rarely targeted at populations considered vulnerable to such environmental perturbations. Here, we assess the level of heritable variation in the ability of embryos to tolerate desiccation stress in Pseudophryne guentheri, a terrestrial-breeding frog that is currently experiencing a drying climate. We applied a North Carolina II breeding design to identify sources of genetic and environmental variance, and genotype-by-environment interactions (GEIs), underlying the expression of embryo survival, hatching times, hatchling mass, size, and shape. Our analysis revealed highly significant effects of water potential and maternal effects on all measured traits, while additive genetic effects were significant for hatchling shape, and nonadditive effects were observed for embryo survival. Interestingly, GEIs, including for some traits complex three-way sire-by-dam-by-environment interactions, were significant, indicating that progeny from certain male-female crosses were more tolerant to water stress than others. These findings suggest a limited capacity of P. guentheri to respond to a drying climate, but also reveal that the detrimental effects of nonviable male-female crosses (i.e., genetic incompatibility) can be masked in benign environments.     

The genetic architecture of maternal effects across ontogeny in the red deer

Maternal effects, either environmental or genetic in origin, are an underappreciated source of phenotypic variance in natural populations. Maternal genetic effects have the potential to constrain or enhance the evolution of offspring traits depending on their magnitude and their genetic correlation with direct genetic effects. We estimated the maternal effect variance and its genetic component for 12 traits expressed over the life history in a pedigreed population of wild red deer (morphology, survival/longevity, breeding success). We only found support for maternal genetic effect variance in the two neonatal morphological traits: birth weight ( = 0.31) and birth leg length ( = 0.17). For these two traits, the genetic correlation between maternal and direct additive effects was not significantly different from zero, indicating no constraint to evolution from genetic architecture. In contrast, variance in maternal genetic effects enhanced the additive genetic variance available to respond to natural selection. Maternal effect variance was negligible for late-life traits. We found no evidence for sex differences in either the direct or maternal genetic architecture of offspring traits. Our results suggest that maternal genetic effect variance declines over the lifetime, but also that this additional heritable genetic variation may facilitate evolutionary responses of early-life traits.     

Genetic architecture of survival and fitness-related traits in two populations of Atlantic salmon

The additive genetic effects of traits can be used to predict evolutionary trajectories, such as responses to selection. Non-additive genetic and maternal environmental effects can also change evolutionary trajectories and influence phenotypes, but these effects have received less attention by researchers. We partitioned the phenotypic variance of survival and fitness-related traits into additive genetic, non-additive genetic and maternal environmental effects using a full-factorial breeding design within two allopatric populations of Atlantic salmon (Salmo salar). Maternal environmental effects were large at early life stages, but decreased during development, with non-additive genetic effects being most significant at later juvenile stages (alevin and fry). Non-additive genetic effects were also, on average, larger than additive genetic effects. The populations, generally, did not differ in the trait values or inferred genetic architecture of the traits. Any differences between the populations for trait values could be explained by maternal environmental effects. We discuss whether the similarities in architectures of these populations is the result of natural selection across a common juvenile environment.     

Environmental effects on the structure of the G‐matrix

Genetic correlations between traits determine the multivariate response to selection in the short term, and thereby play a causal role in evolutionary change. Although individual studies have documented environmentally induced changes in genetic correlations, the nature and extent of environmental effects on multivariate genetic architecture across species and environments remain largely uncharacterized. We reviewed the literature for estimates of the genetic variance–covariance ( G ) matrix in multiple environments, and compared differences in G between environments to the divergence in G between conspecific populations (measured in a common garden). We found that the predicted evolutionary trajectory differed as strongly between environments as it did between populations. Between‐environment differences in the underlying structure of G (total genetic variance and the relative magnitude and orientation of genetic correlations) were equal to or greater than between‐population differences. Neither environmental novelty, nor the difference in mean phenotype predicted these differences in G . Our results suggest that environmental effects on multivariate genetic architecture may be comparable to the divergence that accumulates over dozens or hundreds of generations between populations. We outline avenues of future research to address the limitations of existing data and characterize the extent to which lability in genetic correlations shapes evolution in changing environments.     

Local Adaptation and Genetics of Acid-Stress Tolerance in the Moor Frog, Rana arvalis

As potential to adapt to environmental stress can be essential for population persistence, knowledge on the genetic architecture of local adaptation is important for conservation genetics. We investigated the relative importance of additive genetic, dominance and maternal effects contributions to acid stress tolerance in two moor frog (Rana arvalis) populations originating from low and neutral pH habitats. Experiments with crosses obtained from artificial matings revealed that embryos from the acid origin population were more tolerant to low pH than embryos from the neutral origin population in embryonic survival rates, but not in terms of developmental stability, developmental and growth rates. Strong maternal effect and small additive genetic contributions to variation were detected in all traits in both populations. In general, dominance contributions to variance in different traits were of similar magnitude to the additive genetic effects, but dominance effects outweighed the additive genetic and maternal effects contributions to early growth in both populations. Furthermore, the expression of additive genetic variance was independent of pH treatment, suggesting little additive genetic variation in acid stress tolerance. The results suggest that although local genetic adaptation to acid stress has taken place, the current variation in acid stress tolerance in acidified populations may owe largely to non-genetic effects. However, low but significant heritabilities (h ² 0.07–0.22) in all traits – including viability itself – under a wide range of pH conditions suggests that environmental stress created by low pH is unlikely to lower moor frog populations' ability to respond to selection in the traits studied. Nevertheless, acid conditions could lower populations' ability to respond to selection in the long run through reduction in effective population size.     

Parental effects on embryonic viability and growth in Arctic charr Salvelinus alpinus at two incubation temperatures

The parental influences on three progeny traits (survival to eyed‐embryo stage, post‐hatching body length and yolk‐sac volume) of Arctic charr Salvelinus alpinus were studied under two thermal conditions (2 and 7° C) using a factorial mating design. The higher temperature resulted in elevated mortality rates and less advanced development at hatching. Survival was mostly attributable to maternal effects at both temperatures, but the variation among families was dependent on egg size only at the low temperature. No additive genetic variation (or pure sire effect) could be observed, whereas the non‐additive genetic effects (parental combination) contributed to offspring viability at 2° C. In contrast, any observable genetic variance in survival was lost at 7° C, most likely due to the increased environmental variance. Irrespective of temperature, dam and sire–dam interaction contributed significantly to the phenotypic variation in both larval length and yolk size. A significant proportion of the variation in larval length was also due to the sire effect at 2° C. Maternal effects were mediated partly through egg size, but as a whole, they decreased in importance at the high temperature, enabling a concomitant increase in non‐additive genetic effects. For larval length, however, the additive component, like maternal effects, decreased at 7° C. The present results suggest that an exposure to thermal stress during incubation can modify the genetic architecture of early developmental traits in S. alpinus and presumably constrain their short‐term adaptive potential and evolvability by increasing the amount of environmentally induced variation.     

Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations

Phenotypic plasticity provides means for adapting to environmental unpredictability. In terms of accelerated development in the face of pond-drying risk, phenotypic plasticity has been demonstrated in many amphibian species, but two issues of evolutionary interest remain unexplored. First, the heritable basis of plastic responses is poorly established. Second, it is not known whether interpopulational differences in capacity to respond to pond-drying risk exist, although such differences, when matched with differences in desiccation risk would provide strong evidence for local adaptation. We investigated sources of within- and among-population variation in plastic responses to simulated pond-drying risk (three desiccation treatments) in two Rana temporaria populations originating from contrasting environments: (1) high desiccation risk with weak seasonal time constraint (southern population); and (2) low desiccation risk with severe seasonal time constraint (northern population). The larvae originating from the environment with high desiccation risk responded adaptively to the fast decreasing water treatment by accelerating their development and metamorphosing earlier, but this was not the case in the larvae originating from the environment with low desiccation risk. In both populations, metamorphic size was smaller in the high-desiccation-risk treatment, but the effect was larger in the southern population. Significant additive genetic variation in development rate was found in the northern and was nearly significant in the southern population, but there was no evidence for genetic variation in plasticity for development rates in either of the populations. No genetic variation for plasticity was found either in size at metamorphosis or growth rate. All metamorphic traits were heritable, and additive genetic variances were generally somewhat higher in the southern population, although significantly so in only one trait. Dominance variances were also significant in three of four traits, but the populations did not differ. Maternal effects in metamorphic traits were generally weak in both populations. Within-environment phenotypic correlations between larval period and metamorphic size were positive and genetic correlations negative in both populations. These results suggest that adaptive phenotypic plasticity is not a species-specific fixed trait, but evolution of interpopulational differences in plastic responses are possible, although heritability of plasticity appears to be low. The lack of adaptive response to desiccation risk in northern larvae is consistent with the interpretation that selection imposed by shorter growing season has favored rapid development in north (approximately 8% faster development in north as compared to south) or a minimum metamorphic size at the expense of phenotypic plasticity.     

Body size divergence in nine‐spined sticklebacks: disentangling additive genetic and maternal effects

Interpopulation differences in body size are of common occurrence in vertebrates, but the relative importance of genetic, maternal, and environmental effects as causes of observed differentiation have seldom been assessed in the wild. Gigantism in pond nine‐spined sticklebacks (Pungitius pungitius Linnaeus, 1758) has been repeatedly observed, but the quantitative genetic basis of population divergence in size has remained unstudied. We conducted a common garden experiment – using ‘pure’ and reciprocal crosses between two populations (‘giant’ pond versus ‘normal’ marine) – to test for the relative importance of additive genetic, non‐additive genetic, and maternal effects on body size after 11 months of growth in the laboratory. We found that body size difference between the two populations in laboratory conditions owed mainly to additive genetic effects, and only to a minor degree to maternal effects. Furthermore, the weak maternal effects were seen only in the offspring of ‘giant’ mothers, and appeared to be mediated through differences in egg size. Thus, the results suggest that gigantism in pond populations of P. pungitius is based on the effects of additively acting genes, rather than to direct environmental induction, or maternal or non‐additive gene action. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 521–528.     

Genetic by environmental variation but no local adaptation in oysters (Crassostrea virginica)

Functional trait variation within and across populations can strongly influence population, community, and ecosystem processes, but the relative contributions of genetic vs. environmental factors to this variation are often not clear, potentially complicating conservation and restoration efforts. For example, local adaptation, a particular type of genetic by environmental (G*E) interaction in which the fitness of a population in its own habitat is greater than in other habitats, is often invoked in management practices, even in the absence of supporting evidence. Despite increasing attention to the potential for G*E interactions, few studies have tested multiple populations and environments simultaneously, limiting our understanding of the spatial consistency in patterns of adaptive genetic variation. In addition, few studies explicitly differentiate adaptation in response to predation from other biological and environmental factors. We conducted a reciprocal transplant experiment of first‐generation eastern oyster (Crassostrea virginica) juveniles from six populations across three field sites spanning 1000 km in the southeastern Atlantic Bight in both the presence and absence of predation to test for G*E variation in this economically valuable and ecologically important species. We documented significant G*E variation in survival and growth, yet there was no evidence for local adaptation. Condition varied across oyster cohorts: Offspring of northern populations had better condition than offspring from the center of our region. Oyster populations in the southeastern Atlantic Bight differ in juvenile survival, growth, and condition, yet offspring from local broodstock do not have higher survival or growth than those from farther away. In the absence of population‐specific performance information, oyster restoration and aquaculture may benefit from incorporating multiple populations into their practices.     

Genetic quality and offspring performance in Chinook salmon: implications for supportive breeding

Each year salmon and other fishes are caught and used for supportive breeding programs that attempt to augment natural populations that are threatened with extinction. These programs typically mate individuals randomly and as such they overlook the importance of genetic quality to offspring fitness and ultimately to ensuring population health. Here, we use Chinook salmon (Oncorhynchus tshawytscha) and a fully crossed quantitative genetic breeding design to partition genetic variance in offspring performance (growth and survival) to additive and non-additive genetic effects as well as maternal effects. We show that these three effects contribute about equally to the variation in survival, but only non-additive genetic and maternal effects contribute to variation in growth. Some of the genetic effects could be assigned to variation at the class IIB locus of the major histocompatibility complex, but the maternal effects were not associated with egg size and we found no relationship between dam phenotypic measures and offspring survival or growth. We also found no relationship between sire sexually selected characters and offspring survival or growth, which is inconsistent with a “good genes” hypothesis. Finally, we show that incorporation of genetic quality into supportive breeding programs can increase offspring growth or survival by between 3% and 19% during the endogenous feeding stage alone, and projections to adulthood suggest that survivorship could be over four fold higher. Electronic Supplementary Material  Supplementary material is available in the online version of this article at and is accessible for authorised users.     

Heterogeneity of genetic architecture of body size traits in a free‐living population

Knowledge of the underlying genetic architecture of quantitative traits could aid in understanding how they evolve. In wild populations, it is still largely unknown whether complex traits are polygenic or influenced by few loci with major effect, due to often small sample sizes and low resolution of marker panels. Here, we examine the genetic architecture of five adult body size traits in a free‐living population of Soay sheep on St Kilda using 37 037 polymorphic SNPs. Two traits (jaw and weight) show classical signs of a polygenic trait: the proportion of variance explained by a chromosome was proportional to its length, multiple chromosomes and genomic regions explained significant amounts of phenotypic variance, but no SNPs were associated with trait variance when using GWAS. In comparison, genetic variance for leg length traits (foreleg, hindleg and metacarpal) was disproportionately explained by two SNPs on chromosomes 16 (s23172.1) and 19 (s74894.1), which each explained >10% of the additive genetic variance. After controlling for environmental differences, females heterozygous for s74894.1 produced more lambs and recruits during their lifetime than females homozygous for the common allele conferring long legs. We also demonstrate that alleles conferring shorter legs have likely entered the population through a historic admixture event with the Dunface sheep. In summary, we show that different proxies for body size can have very different genetic architecture and that dense SNP helps in understanding both the mode of selection and the evolutionary history at loci underlying quantitative traits in natural populations.     

Quantitative genetics of seed size variation inPhlox

Summary Because seed size is often associated with survival and reproduction in plant populations, genetic variation for seed size may be reduced or eliminated by natural selection. To test this hypothesis we assessed genetic sources of variation in seed size in a population ofPhlox drummondii to determine whether genetic differences among seeds influence the size they attain. A diallel cross among 12 plants from a population at Bastrop, Texas, USA allowed us to partition variance in the mass of seeds among several genetic and parental effects. We found no evidence of additive genetic variance or dominance genetic variance for seed mass in the contribution of plants to their offspring. Extranuclear maternal effects accounted for 56% of the variance in seed mass. A small interaction was observed between seed genotype and maternal plant. Results of this study support theory that predicts little genetic variation for traits associated with fitness.     

Genetic architecture and phenotypic plasticity of thermally-regulated traits in an eruptive species, <Emphasis Type="Italic">Dendroctonus ponderosae</Emphasis>

Phenotypic plasticity in thermally-regulated traits enables close tracking of changing environmental conditions, and can thereby enhance the potential for rapid population increase, a hallmark of outbreak insect species. In a changing climate, exposure to conditions that exceed the capacity of existing phenotypic plasticity may occur. Combining information on genetic architecture and trait plasticity among populations that are distributed along a latitudinal cline can provide insight into how thermally-regulated traits evolve in divergent environments and the potential for adaptation. Dendroctonus ponderosae feed on Pinus species in diverse climatic regimes throughout western North America, and show eruptive population dynamics. We describe geographical patterns of plasticity in D. ponderosae development time and adult size by examining reaction norms of populations from multiple latitudes. The relative influence of additive and non-additive genetic effects on population differences in the two phenotypic traits at a single temperature is quantified using line-cross experiments and joint-scaling tests. We found significant genetic and phenotypic variation among D. ponderosae populations. Simple additive genetic variance was not the primary source of the observed variation, and dominance and epistasis contributed greatly to the genetic divergence of the two thermally-regulated traits. Hybrid breakdown was also observed in F₂ hybrid crosses between northern and southern populations, further indication of substantial genetic differences among clinal populations and potential reproductive isolation within D. ponderosae. Although it is unclear what maintains variation in the life-history traits, observed plasticity in thermally-regulated traits that are directly linked to rapid numerical change may contribute to the outbreak nature of D. ponderosae, particularly in a changing climate.     

RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY: MATERNAL EFFECTS AND SELECTION ON LIFE-HISTORY CHARACTERS AND PLASTICITIES IN MIMULUS GUTTATUS

Recent studies in plant populations have found that environmental heterogeneity and phenotypic selection vary at local spatial scales. In this study, I ask if there is evolutionary change in response to environmental heterogeneity and, if so, whether the response occurs for characters or character plasticities. I used vegetative clones of Mimulus guttatus to create replicate populations of 75 genotypes. These populations were planted into the natural habitat where they differed in mean growth, flowering phenology, and life span. This phenotypic variation was used to define selective environments. There was variation in fitness (flower production) among genotypes across all planting sites and in genotype response to the selective environment. Offspring from each site were grown in the greenhouse in two water treatments. Because each population initially had the same genetic composition, variation in the progeny between selective environments reveals either evolutionary change in response to environmental heterogeneity or environmental maternal effects. Plants from experimental sites that flowered earlier, had shorter life spans and were less productive, produced offspring that had more flowers, on average, and were less plastic in vegetative allocation than offspring of longer-lived plants from high-productivity areas. However, environmental maternal effects masked phenotypic differences in flower production. Therefore, although there was evidence of genetic differentiation in both life-history characters and their plasticities in response to small-scale environmental heterogeneity, environmental maternal effects may slow evolutionary change. Response to local-scale selective regimes suggests that environmental heterogeneity and local variation in phenotypic selection may act to maintain genetic variation.     

Evolution of Adaptation and Mate Choice: Parental Relatedness Affects Expression of Phenotypic Variance in a Natural Population

Mating between relatives generally results in reduced offspring viability or quality, suggesting that selection should favor behaviors that minimize inbreeding. However, in natural populations where searching is costly or variation among potential mates is limited, inbreeding is often common and may have important consequences for both offspring fitness and phenotypic variation. In particular, offspring morphological variation often increases with greater parental relatedness, yet the source of this variation, and thus its evolutionary significance, are poorly understood. One proposed explanation is that inbreeding influences a developing organism’s sensitivity to its environment and therefore the increased phenotypic variation observed in inbred progeny is due to greater inputs from environmental and maternal sources. Alternatively, changes in phenotypic variation with inbreeding may be due to additive genetic effects alone when heterozygotes are phenotypically intermediate to homozygotes, or effects of inbreeding depression on condition, which can itself affect sensitivity to environmental variation. Here we examine the effect of parental relatedness (as inferred from neutral genetic markers) on heritable and nonheritable components of developmental variation in a wild bird population in which mate choice is often constrained, thereby leading to inbreeding. We found greater morphological variation and distinct contributions of variance components in offspring from highly related parents: inbred offspring tended to have greater environmental and lesser additive genetic variance compared to outbred progeny. The magnitude of this difference was greatest in late-maturing traits, implicating the accumulation of environmental variation as the underlying mechanism. Further, parental relatedness influenced the effect of an important maternal trait (egg size) on offspring development. These results support the hypothesis that inbreeding leads to greater sensitivity of development to environmental variation and maternal effects, suggesting that the evolutionary response to selection will depend strongly on mate choice patterns and population structure.     

Sea ice predicts long‐term trends in Adélie penguin population growth,but not annual fluctuations: Results from a range‐wide multiscale analysis

Understanding the scales at which environmental variability affects populations is critical for projecting population dynamics and species distributions in rapidly changing environments. Here we used a multilevel Bayesian analysis of range‐wide survey data for Adélie penguins to characterize multidecadal and annual effects of sea ice on population growth. We found that mean sea ice concentration at breeding colonies (i.e., “prevailing” environmental conditions) had robust nonlinear effects on multidecadal population trends and explained over 85% of the variance in mean population growth rates among sites. In contrast, despite considerable year‐to‐year fluctuations in abundance at most breeding colonies, annual sea ice fluctuations often explained less than 10% of the temporal variance in population growth rates. Our study provides an understanding of the spatially and temporally dynamic environmental factors that define the range limits of Adélie penguins, further establishing this iconic marine predator as a true sea ice obligate and providing a firm basis for projection under scenarios of future climate change. Yet, given the weak effects of annual sea ice relative to the large unexplained variance in year‐to‐year growth rates, the ability to generate useful short‐term forecasts of Adélie penguin breeding abundance will be extremely limited. Our approach provides a powerful framework for linking short‐ and longer term population processes to environmental conditions that can be applied to any species, facilitating a richer understanding of ecological predictability and sensitivity to global change.