Geographic variation in adult and embryonic desiccation tolerance in a terrestrial-breeding frog

Intraspecific variation in the ability of individuals to tolerate environmental perturbations is often neglected when considering the impacts of climate change. Yet this information is potentially crucial for mitigating deleterious effects of climate change on threatened species. Here we assessed patterns of intraspecific variation in desiccation tolerance in the frog Pseudophryne guentheri, a terrestrial-breeding species experiencing a drying climate. Adult frogs were collected from six populations across a rainfall gradient and their dehydration and rehydration rates were assessed. We also compared desiccation tolerance of embryos and hatchlings originating from within-population parental crosses from four of the populations. Embryos were reared on soil at three soil–water potentials and their desiccation tolerance was assessed across a range of traits. We found significant and strong patterns of intraspecific variation in almost all traits, both in adults and first-generation offspring. Adult frogs exhibited clinal variation in their water balance responses, with populations from drier sites both dehydrating and rehydrating more slowly compared to frogs from more mesic sites. Similarly, desiccation tolerance of first-generation offspring was significantly greater in populations from xeric sites. Our findings suggest that populations within this species will respond differently to the regional reduction in rainfall predicted by climate change models.     

Consequences of genetic erosion on fitness and phenotypic plasticity in European tree frog populations (Hyla arborea)

The detrimental effects of genetic erosion on small isolated populations are widely recognized contrary to their interactions with environmental changes. The ability of genotypes to plastically respond to variability is probably essential for the persistence of these populations. Genetic erosion impact may be exacerbated if inbreeding affects plastic responses or if their maintenance were at higher phenotypic costs. To understand the interplay 'genetic erosion-fitness-phenotypic plasticity', we experimentally compared, in different environments, the larval performances and plastic responses to predation of European tree frogs (Hyla arborea) from isolated and connected populations. Tadpoles from isolated populations were less performant, but the traits affected were environmental dependant. Heterosis observed in crosses between isolated populations allowed attributing their low fitness to inbreeding. Phenotypic plasticity can be maintained in the face of genetic erosion as inducible defences in response to predator were identical in all populations. However, the higher survival and developmental costs for isolated populations in harsh conditions may lead to an additional fitness loss for isolated populations.     

Quantitative trait loci affecting survival and fertility-related traits in Caenorhabditis elegans show genotype-environment interactions, pleiotropy and epistasis.

We have identified, using composite interval mapping, quantitative trait loci (QTL) affecting a variety of life history traits (LHTs) in the nematode Caenorhabditis elegans. Using recombinant inbred strains assayed on the surface of agar plates, we found QTL for survival, early fertility, age of onset of sexual maturity, and population growth rate. There was no overall correlation between survival on solid media and previous measures of survival in liquid media. Of the four survival QTL found in these two environments, two have genotype-environment interactions (GEIs). Epistatic interactions between markers were detected for four traits. A multiple regression approach was used to determine which single markers and epistatic interactions best explained the phenotypic variance for each trait. The amount of phenotypic variance accounted for by genetic effects ranged from 13% (for internal hatching) to 46% (for population growth). Epistatic effects accounted for 9-11% of the phenotypic variance for three traits. Two regions containing QTL that affected more than one fertility-related trait were found. This study serves as an example of the power of QTL mapping for dissecting the genetic architecture of a suite of LHTs and indicates the potential importance of environment and GEIs in the evolution of this architecture.     

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.     

Old wine in new bottles: reaction norms in salmonid fishes

Genetic variability in reaction norms reflects differences in the ability of individuals, populations and ultimately species to respond to environmental change. By increasing our understanding of how genotype × environment interactions influence evolution, studies of genetic variation in phenotypic plasticity serve to refine our capacity to predict how populations will respond to natural and anthropogenic environmental variability, including climate change. Given the extraordinary variability in morphology, behaviour and life history in salmonids, one might anticipate the research milieu on reaction norms in these fishes to be empirically rich and intellectually engaging. Here, I undertake a review of genetic variability in continuous and discontinuous (threshold) norms of reaction in salmonid fishes, as determined primarily (but not exclusively) by common-garden experiments. Although in its infancy from a numerical publication perspective, there is taxonomically broad evidence of genetic differentiation in continuous, threshold and bivariate reaction norms among individuals, families and populations (including inter-population hybrids and backcrosses) for traits as divergent as embryonic development, age and size at maturity, and gene expression. There is compelling inferential evidence that plasticity is heritable and that population differences in reaction norms can reflect adaptive responses, by natural selection, to local environments. As a stimulus for future work, a series of 20 research questions are identified that focus on reaction-norm variability, selection, costs and constraints, demographic and conservation consequences, and genetic markers and correlates of phenotypic plasticity.     

Fluctuations in the incubation moisture environment affect growth but not survival of hatchling lizards

Few studies have collected longitudinal data that follow the complete microevolutionary path of an organism linking sources of variation (e.g. environmental versus genetic) to a trait and its subsequent relationship with fitness. Identifying the links within this pathway is imperative for understanding the ecological relevance of effects found at the phenotypic level. Furthermore, experimental studies that examine parts of the pathway in ectothermic organisms often fail to mimic the complexities of the natural developmental environment. Temperature and moisture conditions in reptile nests, for example, can fluctuate greatly on a seasonal and daily basis. Despite the potential effects of fluctuating environments, the vast majority of studies have held environmental treatments constant during the developmental period. We investigated the effects of fluctuating moisture regimes during incubation on eggs, hatchling phenotypes, and subsequent survival in the eastern fence lizard Sceloporus undulatus. Moisture fluctuations during embryonic development caused water absorption by eggs to follow the environmental availability of moisture. Initial hatchling tail length was affected by the pattern of moisture fluctuations, and hatchling growth rates in fluctuating treatments were significantly faster than those in a constant treatment, resulting in larger hatchlings after 4 weeks. A release–recapture experiment conducted in the field did not detect a treatment effect on survival despite the larger body sizes. In summary, although fluctuations affected water absorption by eggs and some hatchling traits, these effects did not have subsequent fitness consequences. The results obtained suggest that egg and hatchling survival are buffered against natural soil moisture fluctuations during incubation, even when egg and hatchling traits are significantly affected. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 89–102.     

Climate change affects the early-life history of a freshwater turtle in a severely drying region

Freshwater turtles are one of the most threatened vertebrate groups. Climate change is a major threat to these species, with impacts affecting all life-history stages. There is currently a limited understanding of how changes in climate may alter the environmental triggers for hatching and emergence from the nests of freshwater turtle hatchlings. This precludes making predictions about how climate change may impact freshwater turtle recruitment success. The southwestern snake-necked turtle (Chelodina oblonga) is endemic to south-western Australia, a global biodiversity hotspot that has undergone severe climatic drying. Recruitment failure is thought to be occurring in many populations of the species. However, there is little understanding as to how environmental change may be influencing recruitment. This study aimed to: (1) determine the incubation duration and hatching and hatchling emergence success of C. oblonga, (2) determine if the species exhibits hatching or emergence synchrony and/or delayed emergence and (3) quantify the effects of temperature and rainfall on hatchling emergence. Using this information, the study assesses how climatic drying and warming may be impacting C. oblonga's early life-history. Between 2018 and 2020 nest sites were monitored around a large urban wetland with weekly assessments of egg and hatchling status. Incubation duration and hatching and hatchling emergence success were calculated, and generalized linear models were built to determine how temperature and/or rainfall predicted emergence. Hatchlings either emerged shortly after hatching or overwintered in the nest, and both hatching and emergence were asynchronous. Both emergence periods were positively associated with temperature and rainfall. This study reveals that incubation duration, hatching success, hatchling emergence and survival are all likely to be impacted by recent and projected climate change, and especially drying. Warming and drying are predicted for many temperate regions globally, and it is therefore important that their impacts on the early life history of freshwater turtles be better understood.     

Latitudinal and temperature-dependent variation in embryonic development and growth in Rana temporaria

Variation in seasonal time constraints and temperature along latitudinal gradients are expected to select for life history trait differentiation, but information about the relative importance of these factors in shaping patterns of divergence in embryonic traits remains sparse. We studied embryonic survival, growth and development rates in the common frog (Rana temporaria) along a 1,400-km latitudinal gradient across Sweden by raising embryos from four populations in the laboratory at seven temperatures (9 degrees C, 12 degrees C, 15 degrees C, 18 degrees C, 21 degrees C, 24 degrees C, 27 degrees C). We found significant differences in mean values of all traits between the populations and temperature treatments, but this variation was not latitudinally ordered. In general, embryonic survival decreased at the two highest temperatures in all populations, but less so in the southernmost as compared to the other populations. The northernmost population developed slowest at the lowest temperature, while the two mid-latitude populations were slowest at the other temperatures. Hatchling size increased with increasing temperature especially in the two northern populations, whereas the two southern populations showed peak hatchling size at 15 degrees C. Analyses of within-population genetic variation with a half-sib design revealed that there was significant additive genetic variation in all traits, and egg size-related maternal effects were important in the case of hatchling size. Overall, our results indicate that unlike larval growth and development, variation in embryonic development and growth in R. temporaria cannot be explained in terms of a latitudinal gradient in season length. While adaptation to a latitudinal variation in temperature might have contributed to the observed differentiation in embryonic performance, the effects of other, perhaps more local environmental factors, seem to have overridden them in importance.     

Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits

The relative importance of genetic, environmental, and maternal effects as determinants of geographical variation in vertebrate life-histories has not often been explored. We examined the role of genetic and maternal effects as determinants of population divergence in survival and three important larval life-history traits (growth rate, age, and size at metamorphosis) using reciprocal crosses between two latitudinally separated populations of the common frog ( Rana temporaria Linnaeus). Genetic effects were important in all three traits as indicated by the significant effect of male origin, but there was also evidence for nonadditive genetic contributions on metamorphic size and growth rate. Likewise, maternal effect contributions to population divergence were large, partially environment dependent, and apparently acting primarily through egg size in two of three traits. These results suggest that both genetic and maternal effects are important determinants of geographical variation in amphibian life-histories, and that much of the differentiation resulting from maternal effects is mediated through variation in egg size. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 61–70.     

Life-history consequences of egg size in Drosophila melanogaster

We used a novel approach to study the effects of egg size on offspring fitness components in Drosophila melanogaster. Populations that differed genetically in egg size were crossed, and the female offspring from these reciprocal crosses were examined for life-history traits. These flies expressed effects of egg size, because they developed from eggs of different sizes as a result of maternal genetic effects, but displayed an equivalent range of nuclear genetic variation. The crosses used four independent pairs of outbred populations that differed in the pattern of covariation between egg size and life-history traits, so that the maternal genetic effects of egg size on offspring characters could be contrasted to the associations present among the parental populations. Egg size showed positive maternal genetic effects on embryonic viability and development rate, hatchling weight and feeding rate, and egg-larva and egg-adult development rate but no consistent effects on larval competitive ability, adult weight, or egg size in the offspring. Our method revealed a pattern of causality that could not be deduced from interpopulation comparisons and therefore provides a good way of disentangling the causes and consequences of variation in egg size while controlling for zygotic genetic effects.     

Accounting for Population Structure in Gene-by-Environment Interactions in Genome-Wide Association Studies Using Mixed Models

Although genome-wide association studies (GWASs) have discovered numerous novel genetic variants associated with many complex traits and diseases, those genetic variants typically explain only a small fraction of phenotypic variance. Factors that account for phenotypic variance include environmental factors and gene-by-environment interactions (GEIs). Recently, several studies have conducted genome-wide gene-by-environment association analyses and demonstrated important roles of GEIs in complex traits. One of the main challenges in these association studies is to control effects of population structure that may cause spurious associations. Many studies have analyzed how population structure influences statistics of genetic variants and developed several statistical approaches to correct for population structure. However, the impact of population structure on GEI statistics in GWASs has not been extensively studied and nor have there been methods designed to correct for population structure on GEI statistics. In this paper, we show both analytically and empirically that population structure may cause spurious GEIs and use both simulation and two GWAS datasets to support our finding. We propose a statistical approach based on mixed models to account for population structure on GEI statistics. We find that our approach effectively controls population structure on statistics for GEIs as well as for genetic variants.     

A genome‐wide search for local adaptation in a terrestrial‐breeding frog reveals vulnerability to climate change

Terrestrial‐breeding amphibians are likely to be vulnerable to warming and drying climates, as their embryos require consistent moisture for successful development. Adaptation to environmental change will depend on sufficient genetic variation existing within or between connected populations. Here, we use Single Nucleotide Polymorphism (SNP) data to investigate genome‐wide patterns in genetic diversity, gene flow and local adaptation in a terrestrial‐breeding frog (Pseudophryne guentheri) subject to a rapidly drying climate and recent habitat fragmentation. The species was sampled across 12 central and range‐edge populations (192 samples), and strong genetic structure was apparent, as were high inbreeding coefficients. Populations showed differences in genetic diversity, and one population lost significant genetic diversity in a decade. More than 500 SNP loci were putatively under directional selection, and 413 of these loci were correlated with environmental variables such as temperature, rainfall, evaporation and soil moisture. One locus showed homology to a gene involved in the activation of maturation in Xenopus oocytes, which may facilitate rapid development of embryos in drier climates. The low genetic diversity, strong population structuring and presence of local adaptation revealed in this study shows why management strategies such as targeted gene flow may be necessary to assist isolated populations to adapt to future climates.     

Latitudinal and voltinism compensation shape thermal reaction norms for growth rate

Latitudinal variation in thermal reaction norms of key fitness traits may inform about the response of populations to climate warming, yet their adaptive nature and evolutionary potential are poorly known. We assessed the contribution of quantitative genetic, neutral genetic and environmental effects to thermal reaction norms of growth rate for populations of the damselfly Ischnura elegans. Among populations, reaction norms differed primarily in elevation, suggesting that time constraints associated with shorter growth seasons in univoltine, high-latitude as well as multivoltine, low-latitude populations selected for faster growth rates. Phenotypic divergence among populations is consistent with selection rather than drift as Q(ST) was greater than F(ST) in all cases. Q(ST) estimates increased with experimental temperature and were influenced by genotype by environment interactions. Substantial additive genetic variation for growth rate in all populations suggests that evolution of trait means in different environments is not constrained. Heritability of growth rates was higher at high temperature, driven by increased genetic rather than environmental variance. While environment-specific nonadditive effects also may contribute to heritability differences among temperatures, maternal effects did not play a significant role (where these could be accounted for). Genotype by environment interactions strongly influenced the adaptive potential of populations, and our results suggest the potential for microevolution of thermal reaction norms in each of the studied populations. In summary, the observed latitudinal pattern in growth rates is adaptive and results from a combination of latitudinal and voltinism compensation. Combined with the evolutionary potential of thermal reaction norms, this may affect populations' ability to respond to future climate warming.     

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.     

Testing population differentiation in plant species – how important are environmental maternal effects

The maternal environment may contribute to population differentiation in offspring traits if growing conditions of mother plants are different. However, the magnitude of such environmental maternal effects compared with genetic differentiation is often not clear. We tested the importance of environmental maternal effects by comparing population differentiation in parental seed directly collected in the field and in F₁ seed grown under homogeneous conditions. The F₁ seeds were obtained by random crosses within populations. We used five populations in each of four plant species to analyse seed mass and growth chamber germination of both generations at the same time. In two species, we additionally tested offspring performance in the field. We found a significant population differentiation in all species and for nearly all measured traits. Population‐by‐generation interactions indicating environmental maternal effects were significant for germination (three species) and for seed mass (two species) but not for growth and reproduction. The significant interaction was partly due to a reduction of among‐population differentiation from the parental to the F₁ generation that can be explained by a decrease of maternal provisioning effects. However, in some species by trait combinations a change in population ranking and not a decrease of variation was responsible for significant population‐by‐generation interactions indicating environmental maternal effects beyond maternal provisioning. Fitting of seed mass as covariate was not successful in reducing environmental maternal effects on population differentiation in germination. We discuss alternative methods to account for environmental maternal effects in studies on genetic differentiation among populations.     

Quantitative genetic and translocation experiments reveal genotype‐by‐environment effects on juvenile life‐history traits in two populations of Chinook salmon (Oncorhynchus tshawytscha)

Understanding the genetic architecture of phenotypic plasticity is required to assess how populations might respond to heterogeneous or changing environments. Although several studies have examined population‐level patterns in environmental heterogeneity and plasticity, few studies have examined individual‐level variation in plasticity. Here, we use the North Carolina II breeding design and translocation experiments between two populations of Chinook salmon to detail the genetic architecture and plasticity of offspring survival and growth. We followed the survival of 50 800 offspring through the larval stage and used parentage analysis to examine survival and growth through freshwater rearing. In one population, we found that additive genetic, nonadditive genetic and maternal effects explained 25%, 34% and 55% of the variance in larvae survival, respectively. In the second population, these effects explained 0%, 24% and 61% of the variance in larvae survival. In contrast, fry survival was regulated primarily by additive genetic effects, which indicates a shift from maternal to genetic effects as development proceeds. Fry growth also showed strong additive genetic effects. Translocations between populations revealed that offspring survival and growth varied between environments, the degree of which differed among families. These results indicate genetic differences among individuals in their degree of plasticity and consequently their ability to respond to environmental variation.     

Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaceae)

The genetic background of transplants used to create or augment wild populations may affect the long-term success of restored populations. If seed sources are from differently adapted populations, then the relative performance of progeny from crosses among populations may decrease with an increase in genetic differences of parents and in the differences of parental environments to the transplant location. We evaluated the potential for such outbreeding depression by hybridizing individuals from six different populations of Lotus scoparius var. scoparius and L. s. var. brevialatus. We used allozyme data to calculate genetic distances between source populations, and compiled climatic data and measured soil traits to estimate environmental distances between source populations. We found significant outbreeding depression following controlled crosses. In the greenhouse, the success of crosses (seeds/flower × seedlings/seed) decreased with increasing genetic distance between populations revealing genetically based outbreeding depression unrelated to local adaptation. After outplanting to one native site (in situ common garden), field cumulative fitness of progeny (survival × fruit production) decreased significantly with mean environmental distance of the parental populations to the transplant site, but not with genetic distance between the crossed populations. This result is consistent with a disruption of local adaptation. At the second, ecologically contrasting common garden, where low survival reduced statistical power, field cumulative fitness (survival × progeny height) did not decrease significantly with either environmental distance or genetic distance. Overall, intervariety crosses were 40 and 50% as fit (seeds/flower × seedlings/seed × survival × fruits at the first garden or × height at the second) as intravariety crosses. These results suggest that the cumulative outbreeding depression was caused by a combination of genetically based ecological differences among populations and other genomic coadaptation. We conclude that mixing genetically differentiated seed sources of Lotus scoparius may significantly lower the fitness of augmented or restored populations. Genetic and environmental similarities of source populations relative to the transplant site should be considered when choosing source materials, a practice recommended by recent seed transfer policies. Geographic separation was not a good surrogate for either of these measures.     

Quantitative genetics of larval life-history traits in Rana temporaria in different environmental conditions

The degree to which genetic variation in a given trait varies among different populations of the same species and across different environments has seldom been quantified in wild vertebrate species. We investigated the expression of genetic variability and maternal effects in three larval life-history traits of the amphibian Rana temporaria. In a factorial laboratory experiment, five widely separated populations (max. 1600 km) were subjected to two different environmental treatments. Animal model analyses revealed that all traits were heritable (h(2) approximately 0.20) in all populations and under most treatment combinations. Although the cross-food treatment genetic correlations were close to unity, heritabilities under a restricted food regime tended to be lower than those under an ad libitum food regime. Likewise, maternal effects (m(2) approximately 0.05) were detected in most traits, and they tended to be most pronounced under restricted food conditions. We detected several cross-temperature genetic and maternal effects correlations that were lower than unity, suggesting that genotype-environment interactions and maternal effect-environment interactions are a significant source of phenotypic variation. The results reinforce the perspective that although the expression of genetic and maternal effects may be relatively homogeneous across different populations of the same species, local variation in environmental conditions can lead to significant variation in phenotypic expression of quantitative traits through genotype-environment and maternal effect-environment interactions.     

Genetic and environmental influences on shape variation in the European sea bass (Dicentrarchus labrax)

This paper demonstrates the contribution of both genetic and environmental effects on cultured European sea bass shape. We used the progeny of five populations of sea bass, in a partly diallel design, to investigate the genetics of shape (estimated with geometric morphometrics) in European sea bass. This was done using a common garden experiment with microsatellite markers assignment to parents and populations to avoid confusion between genetic and environmental effects. Additionally, one of the populations was studied over four different aquaculture facilities to investigate the effects of environment on shape. For the first time in this species, shape‐related traits were linked with genetic variation. The first relative warp analysis axis clearly differentiated rearing sites, demonstrating that the main shape/weight effects are related to culturing conditions, thereby accounting for ecomorphologically related differences. The second axis strongly differentiated groups by parental origins; there was a good correlation between shape differences and geographic distances between broodstock sampling locations. High heritabilities of axes scores (0.40–0.55) showed high genetic variation for shape within populations. This study shows that variation in shape has a high genetic component in sea bass, both at the population level and within populations. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 427–436.