Genetic and morphological divergence between Littorina fabalis ecotypes in Northern Europe.

Low dispersal marine intertidal species facing strong divergent selective pressures associated with steep environmental gradients have a great potential to inform us about local adaptation and reproductive isolation. Among these, gastropods of the genus Littorina offer a unique system to study parallel phenotypic divergence resulting from adaptation to different habitats related with wave exposure. In this study, we focused on two Littorina fabalis ecotypes from Northern European shores and compared patterns of habitat-related phenotypic and genetic divergence across three different geographic levels (local, regional and global). Geometric morphometric analyses revealed that individuals from habitats moderately exposed to waves usually present a larger shell size with a wider aperture than those from sheltered habitats. The phenotypic clustering of L. fabalis by habitat across most locations (mainly in terms of shell size) support an important role of ecology in morphological divergence. A genome scan based on amplified fragment length polymorphisms (AFLPs) revealed a heterogeneous pattern of differentiation across the genome between populations from the two different habitats, suggesting ecotype divergence in the presence of gene flow. The contrasting patterns of genetic structure between nonoutlier and outlier loci, and the decreased sharing of outlier loci with geographic distance among locations are compatible with parallel evolution of phenotypic divergence, with an important contribution of gene flow and/or ancestral variation. In the future, model-based inference studies based on sequence data across the entire genome will help unravelling these evolutionary hypotheses, improving our knowledge about adaptation and its influence on diversification within the marine realm.

Postglacial ecotype formation under outcrossing and self-fertilization in Arabidopsis lyrata.

The formation of ecotypes has been invoked as an important driver of postglacial biodiversity, because many species colonized heterogeneous habitats and experienced divergent selection. Ecotype formation has been predominantly studied in outcrossing taxa, while far less attention has been paid to the implications of mating system shifts. Here, we addressed whether substrate-related ecotypes exist in selfing and outcrossing populations of Arabidopsis lyrata subsp. lyrata and whether the genomic footprint differs between mating systems. The North American subspecies colonized both rocky and sandy habitats during postglacial range expansion and shifted the mating system from predominantly outcrossing to predominantly selfing in a number of regions. We performed an association study on pooled whole-genome sequence data of 20 selfing or outcrossing populations, which suggested genes involved in adaptation to substrate. Motivated by enriched gene ontology terms, we compared root growth between plants from the two substrates in a common environment and found that plants originating from sand grew roots faster and produced more side roots, independent of mating system. Furthermore, single nucleotide polymorphisms associated with substrate-related ecotypes were more clustered among selfing populations. Our study provides evidence for substrate-related ecotypes in A. lyrata and divergence in the genomic footprint between mating systems. The latter is the likely result of selfing populations having experienced divergent selection on larger genomic regions due to higher genome-wide linkage disequilibrium.

The predictability and magnitude of life-history divergence to ecological agents of selection: a meta-analysis in livebearing fishes.

Environments causing variation in age-specific mortality - ecological agents of selection - mediate the evolution of reproductive life-history traits. However, the relative magnitude of life-history divergence across selective agents, whether divergence in response to specific selective agents is consistent across taxa and whether it occurs as predicted by theory, remains largely unexplored. We evaluated divergence in offspring size, offspring number, and the trade-off between these traits using a meta-analysis in livebearing fishes (Poeciliidae). Life-history divergence was consistent and predictable to some (predation, hydrogen sulphide) but not all (density, food limitation, salinity) selective agents. In contrast, magnitudes of divergence among selective agents were similar. Finally, there was a negative, asymmetric relationship between offspring-number and offspring-size divergence, suggesting greater costs of increasing offspring size than number. Ultimately, these results provide strong evidence for predictable and consistent patterns of reproductive life-history divergence and highlight the importance of comparing phenotypic divergence across species and ecological selective agents.

Predator-driven intra-species variation in locomotion, metabolism and water velocity preference in pale chub (Zacco platypus) along a river.

Fish inhabit environments that vary greatly in terms of predation intensity, and these predation regimes are generally expected to be a major driver of divergent natural selection. To test whether there is predator-driven intra-species variation in the locomotion, metabolism and water velocity preference of pale chub (Zacco platypus) along a river, we measured unsteady and steady swimming and water velocity preference among fish collected from both high- and low-predation habitats in the Wujiang River. We also measured the routine metabolic rate (RMR), maximum metabolic rate (MMR) and cost of transport (COT) and calculated the optimal swimming speed (Uopt). The fish from the high-predation populations showed a shorter response latency, elevated routine metabolism, lower swimming efficiency at low swimming speed and lower water velocity preference compared with those from the low-predation populations. Neither of the kinematic parameters fast-start and critical swimming speed (Ucrit) showed a significant difference between the high- and low-predation populations. The fish from the high-predation populations may improve their predator avoidance capacity primarily through an elevated routine metabolism and shorter response latency to achieve advanced warning and escape, rather than an improved fast-start swimming speed or acceleration. Thus, the cost of this strategy is an elevated RMR, and no trade-off between unsteady and steady swimming performance was observed in the pale chub population under various predation stresses. It was interesting to find that the high-predation fish showed an unexpected lower velocity preference, which might represent a compromise between predation avoidance, foraging and energy saving.

Colonisation of toxic environments drives predictable life-history evolution in livebearing fishes (Poeciliidae).

New World livebearing fishes (family Poeciliidae) have repeatedly colonised toxic, hydrogen sulphide-rich waters across their natural distribution. Physiological considerations and life-history theory predict that these adverse conditions should favour the evolution of larger offspring. Here, we examined nine poeciliid species that independently colonised toxic environments, and show that these fishes have indeed repeatedly evolved much larger offspring size at birth in sulphidic waters, thus uncovering a widespread pattern of predictable evolution. However, a second pattern, only indirectly predicted by theory, proved additionally common: a reduction in the number of offspring carried per clutch (i.e. lower fecundity). Our analyses reveal that this secondary pattern represents a mere consequence of a classic life-history trade-off combined with strong selection on offspring size alone. With such strong natural selection in extreme environments, extremophile organisms may commonly exhibit multivariate phenotypic shifts even though not all diverging traits necessarily represent adaptations to the extreme conditions.

Do differences in developmental mode shape the potential for local adaptation?

Future climate change is leading to the redistribution of life on Earth as species struggle to cope with rising temperatures. Local adaptation allows species to become locally optimized and persist despite environmental selection, but the extent to which this occurs in nature may be limited by dispersal and gene flow. Congeneric marine gastropod species (Littorina littorea and L. saxatilis) with markedly different developmental modes were collected from across a latitudinal thermal gradient to explore the prevalence of local adaptation to temperature. The acute response of metabolic rate (using oxygen consumption as a proxy) to up-ramping and down-ramping temperature regimes between 6°C and 36°C was quantified for five populations of each species. The highly dispersive L. littorea exhibited minimal evidence of local adaptation to the thermal gradient, with no change in thermal optimum (Topt ) or thermal breadth (Tbr ) and a decline in maximal performance (max ) with increasing latitude. In contrast, the direct developing L. saxatilis displayed evidence of local optimization, although these varied idiosyncratically with latitude, suggesting a suite of selective pressures may be involved in shaping thermal physiology in this relatively sedentary species. Our results show that the biogeography of thermal traits can differ significantly between related species, and show that interpopulation differences in thermal performance do not necessarily follow simple patterns that may be predicted based on latitudinal changes in environmental temperatures. Further research is clearly required to understand the mechanisms that can lead to the emergence of local adaptation in marine systems better and allow improved predictions of species redistribution in response to climate change.

Adaptive divergence in resistance to herbivores in Datura stramonium.

Defensive traits exhibited by plants vary widely across populations. Heritable phenotypic differentiation is likely to be produced by genetic drift and spatially restricted gene flow between populations. However, spatially variable selection exerted by herbivores may also give rise to differences among populations. To explore to what extent these factors promote the among-population differentiation of plant resistance of 13 populations of Datura stramonium, we compared the degree of phenotypic differentiation (P ST) of leaf resistance traits (trichome density, atropine and scopolamine concentration) against neutral genetic differentiation (F ST) at microsatellite loci. Results showed that phenotypic differentiation in defensive traits among-population is not consistent with divergence promoted by genetic drift and restricted gene flow alone. Phenotypic differentiation in scopolamine concentration was significantly higher than F ST across the range of trait heritability values. In contrast, genetic differentiation in trichome density was different from F ST only when heritability was very low. On the other hand, differentiation in atropine concentration differed from the neutral expectation when heritability was less than or equal to 0.3. In addition, we did not find a significant correlation between pair-wise neutral genetic distances and distances of phenotypic resistance traits. Our findings reinforce previous evidence that divergent natural selection exerted by herbivores has promoted the among-population phenotypic differentiation of defensive traits in D. stramonium.

Contemporary and historical evolutionary processes interact to shape patterns of within-lake phenotypic divergences in polyphenic pumpkinseed sunfish, Lepomis gibbosus.

Historical and contemporary evolutionary processes can both contribute to patterns of phenotypic variation among populations of a species. Recent studies are revealing how interactions between historical and contemporary processes better explain observed patterns of phenotypic divergence than either process alone. Here, we investigate the roles of evolutionary history and adaptation to current environmental conditions in structuring phenotypic variation among polyphenic populations of sunfish inhabiting 12 postglacial lakes in eastern North America. The pumpkinseed sunfish polyphenism includes sympatric ecomorphs specialized for littoral or pelagic lake habitats. First, we use population genetic methods to test the evolutionary independence of within-lake phenotypic divergences of ecomorphs and to describe patterns of genetic structure among lake populations that clustered into three geographical groupings. We then used multivariate analysis of covariance (MANCOVA) to partition body shape variation (quantified with geometric morphometrics) among the effects of evolutionary history (reflecting phenotypic variation among genetic clusters), the shared phenotypic response of all populations to alternate habitats within lakes (reflecting adaptation to contemporary conditions), and unique phenotypic responses to habitats within lakes nested within genetic clusters. All effects had a significant influence on body form, but the effects of history and the interaction between history and contemporary habitat were larger than contemporary processes in structuring phenotypic variation. This highlights how divergence can be better understood against a known backdrop of evolutionary history.