Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish

Variation in gene expression contributes to ecological speciation by facilitating population persistence in novel environments. Likewise, immune responses can be of relevance in speciation driven by adaptation to different environments. Previous studies examining gene expression differences between recently diverged ecotypes have often relied on only one pair of populations, targeted the expression of only a subset of genes or used wild‐caught individuals. Here, we investigated the contribution of habitat‐specific parasites and symbionts and the underlying immunological abilities of ecotype hosts to adaptive divergence in lake–river population pairs of the cichlid fish Astatotilapia burtoni. To shed light on the role of phenotypic plasticity in adaptive divergence, we compared parasite and microbiota communities, immune response, and gene expression patterns of fish from natural habitats and a lake‐like pond set‐up. In all investigated population pairs, lake fish were more heavily parasitized than river fish, in terms of both parasite taxon composition and infection abundance. The innate immune response in the wild was higher in lake than in river populations and was elevated in a river population exposed to lake parasites in the pond set‐up. Environmental differences between lake and river habitat and their distinct parasite communities have shaped differential gene expression, involving genes functioning in osmoregulation and immune response. Most changes in gene expression between lake and river samples in the wild and in the pond set‐up were based on a plastic response. Finally, gene expression and bacterial communities of wild‐caught individuals and individuals acclimatized to lake‐like pond conditions showed shifts underlying adaptive phenotypic plasticity.     

Does plasticity enhance or dampen phenotypic parallelism? A test with three lake–stream stickleback pairs

Parallel (and convergent) phenotypic variation is most often studied in the wild, where it is difficult to disentangle genetic vs. environmentally induced effects. As a result, the potential contributions of phenotypic plasticity to parallelism (and nonparallelism) are rarely evaluated in a formal sense. Phenotypic parallelism could be enhanced by plasticity that causes stronger parallelism across populations in the wild than would be expected from genetic differences alone. Phenotypic parallelism could be dampened if site‐specific plasticity induced differences between otherwise genetically parallel populations. We used a common‐garden study of three independent lake–stream stickleback population pairs to evaluate the extent to which adaptive divergence has a genetic or plastic basis, and to investigate the enhancing vs. dampening effects of plasticity on phenotypic parallelism. We found that lake–stream differences in most traits had a genetic basis, but that several traits also showed contributions from plasticity. Moreover, plasticity was much more prevalent in one watershed than in the other two. In most cases, plasticity enhanced phenotypic parallelism, whereas in a few cases, plasticity had a dampening effect. Genetic and plastic contributions to divergence seem to play a complimentary, likely adaptive, role in phenotypic parallelism of lake–stream stickleback. These findings highlight the value of formally comparing wild‐caught and laboratory‐reared individuals in the study of phenotypic parallelism.     

DISENTANGLING THE ROLE OF PHENOTYPIC PLASTICITY AND GENETIC DIVERGENCE IN CONTEMPORARY ECOTYPE FORMATION DURING A BIOLOGICAL INVASION

The occurrence of contemporary ecotype formation through adaptive divergence of populations within the range of an invasive species typically requires standing genetic variation but can be facilitated by phenotypic plasticity. The relative contributions of both of these to adaptive trait differentiation have rarely been simultaneously quantified in recently diverging vertebrate populations. Here we study a case of intraspecific divergence into distinct lake and stream ecotypes of threespine stickleback that evolved in the past 140 years within the invasive range in Switzerland. Using a controlled laboratory experiment with full‐sib crosses and treatments mimicking a key feature of ecotypic niche divergence, we test if the phenotypic divergence that we observe in the wild results from phenotypic plasticity or divergent genetic predisposition. Our experimental groups show qualitatively similar phenotypic divergence as those observed among wild adults. The relative contribution of plasticity and divergent genetic predisposition differs among the traits studied, with traits related to the biomechanics of feeding showing a stronger genetic predisposition, whereas traits related to locomotion are mainly plastic. These results implicate that phenotypic plasticity and standing genetic variation interacted during contemporary ecotype formation in this case.     

Evidence of Adaptive Evolutionary Divergence during Biological Invasion

Rapid phenotypic diversification during biological invasions can either arise by adaptation to alternative environments or by adaptive phenotypic plasticity. Where experimental evidence for adaptive plasticity is common, support for evolutionary diversification is rare. Here, we performed a controlled laboratory experiment using full-sib crosses between ecologically divergent threespine stickleback populations to test for a genetic basis of adaptation. Our populations are from two very different habitats, lake and stream, of a recently invaded range in Switzerland and differ in ecologically relevant morphological traits. We found that in a lake-like food treatment lake fish grow faster than stream fish, resembling the difference among wild type individuals. In contrast, in a stream-like food treatment individuals from both populations grow similarly. Our experimental data suggest that genetically determined diversification has occurred within less than 140 years after the arrival of stickleback in our studied region.     

Phenotypic plasticity and local adaptation favor range expansion of a Neotropical palm

One of the most intriguing questions in plant ecology is which evolutionary strategy allows widely distributed species to increase their ecological range and grow in changing environmental conditions. Phenotypic plasticity and local adaptations are major processes governing species range margins, but little is known about their relative contribution for tree species distribution in tropical forest regions. We investigated the relative role of phenotypic plasticity and local adaptation in the ecological distribution of the widespread palm Euterpe edulis in the Brazilian Atlantic Forest. Genetic sampling and experiments were performed in old‐growth remnants of two forest types with higher (Seasonal Semideciduous Forests vs. Submontane Rainforest) and lower biogeographic association and environmental similarities (Submontane Rainforest vs. Restinga Forest). We first assessed the molecular genetic differentiation among populations, focusing on the group of loci potentially under selection in each forest, using single‐nucleotide polymorphism (SNPs) outliers. Further, we looked for potential adaptive divergence among populations in a common garden experiment and in reciprocal transplants for two plant development phases: seedling establishment and sapling growth. Analysis with outlier loci indicated that all individuals from the Semideciduous Forest formed a single group, while another group was formed by overlapping individuals from Submontane Rainforest and Restinga Forest. Molecular differentiation was corroborated by reciprocal transplants, which yielded strong evidence of local adaptations for seedling establishment in the biogeographically divergent Rainforest and Semideciduous Forest, but not for Restinga Forest and Submontane Rainforest. Phenotypic plasticity for palm seedling establishment favors range expansion to biogeographically related or recently colonized forest types, while persistence in the newly colonized ecosystem may be favored by local adaptations if climatic conditions diverge over time, reducing gene flow between populations. SNPs obtained by next‐generation sequencing can help exploring adaptive genetic variation in tropical trees, which impose several challenges to the use of reciprocal transplants.     

Diversification across a heterogeneous landscape

Adaptation to contrasting environments across a heterogeneous landscape favors the formation of ecotypes by promoting ecological divergence. Patterns of fitness variation in the field can show whether natural selection drives local adaptation and ecotype formation. However, to demonstrate a link between ecological divergence and speciation, local adaptation must have consequences for reproductive isolation. Using contrasting ecotypes of an Australian wildflower, Senecio lautus in common garden experiments, hybridization experiments, and reciprocal transplants, we assessed how the environment shapes patterns of adaptation and the consequences of adaptive divergence for reproductive isolation. Local adaptation was strong between ecotypes, but weaker between populations of the same ecotype. F1 hybrids exhibited heterosis, but crosses involving one native parent performed better than those with two foreign parents. In a common garden experiment, F2 hybrids exhibited reduced fitness compared to parentals and F1 hybrids, suggesting that few genetic incompatibilities have accumulated between populations adapted to contrasting environments. Our results show how ecological differences across the landscape have created complex patterns of local adaptation and reproductive isolation, suggesting that divergent natural selection has played a fundamental role in the early stages of species diversification.     

Geographic variation in phenotypic plasticity in response to dissolved oxygen in an African cichlid fish

Genetic adaptation and phenotypic plasticity are two ways in which organisms can adapt to local environmental conditions. We examined genetic and plastic variation in gill and brain size among swamp (low oxygen; hypoxic) and river (normal oxygen; normoxic) populations of an African cichlid fish, Pseudocrenilabrus multicolor victoriae. Larger gills and smaller brains should be advantageous when oxygen is low, and we hypothesized that the relative contribution of local genetic adaptation vs. phenotypic plasticity should be related to potential for dispersal between environments (because of gene flow’s constraint on local genetic adaptation). We conducted a laboratory‐rearing experiment, with broods from multiple populations raised under high‐oxygen and low‐oxygen conditions. We found that most of the variation in gill size was because of plasticity. However, both plastic and genetic effects on brain mass were detected, as were genetic effects on brain mass plasticity. F₁ offspring from populations with the highest potential for dispersal between environments had characteristically smaller and more plastic brains. This phenotypic pattern might be adaptive in the face of gene flow, if smaller brains and increased plasticity confer higher average fitness across environment types.     

Geographic variation in thermal sensitivity of early life traits in a widespread reptile

Taxa with large geographic distributions generally encompass diverse macroclimatic conditions, potentially requiring local adaptation and/or phenotypic plasticity to match their phenotypes to differing environments. These eco‐evolutionary processes are of particular interest in organisms with traits that are directly affected by temperature, such as embryonic development in oviparous ectotherms. Here we examine the spatial distribution of fitness‐related early life phenotypes across the range of a widespread vertebrate, the painted turtle (Chrysemys picta). We quantified embryonic and hatchling traits from seven locations (in Idaho, Minnesota, Oregon, Illinois, Nebraska, Kansas, and New Mexico) after incubating eggs under constant conditions across a series of environmentally relevant temperatures. Thermal reaction norms for incubation duration and hatchling mass varied among locations under this common‐garden experiment, indicating genetic differentiation or pre‐ovulatory maternal effects. However, latitude, a commonly used proxy for geographic variation, was not a strong predictor of these geographic differences. Our findings suggest that this macroclimatic proxy may be an unreliable surrogate for microclimatic conditions experienced locally in nests. Instead, complex interactions between abiotic and biotic factors likely drive among‐population phenotypic variation in this system. Understanding spatial variation in key life‐history traits provides an important perspective on adaptation to contemporary and future climatic conditions.     

Potential adaptive divergence between subspecies and populations of snapdragon plants inferred from QST–FST comparisons

Phenotypic divergence among natural populations can be explained by natural selection or by neutral processes such as drift. Many examples in the literature compare putatively neutral (F_ST) and quantitative genetic (Q_ST) differentiation in multiple populations to assess their evolutionary signature and identify candidate traits involved with local adaptation. Investigating these signatures in closely related or recently diversified species has the potential to shed light on the divergence processes acting at the interspecific level. Here, we conducted this comparison in two subspecies of snapdragon plants (eight populations of Antirrhinum majus pseudomajus and five populations of A. m. striatum) in a common garden experiment. We also tested whether altitude was involved with population phenotypic divergence. Our results identified candidate phenological and morphological traits involved with local adaptation. Most of these traits were identified in one subspecies but not the other. Phenotypic divergence increased with altitude for a few biomass‐related traits, but only in A. m. striatum. These traits therefore potentially reflect A. m. striatum adaptation to altitude. Our findings imply that adaptive processes potentially differ at the scale of A. majus subspecies.     

Trade‐offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans

Temperature is one of the most important environmental parameters with crucial impacts on nearly all biological processes. Due to anthropogenic activity, average air temperatures are expected to increase by a few degrees in coming decades, accompanied by an increased occurrence of extreme temperature events. Such global trends are likely to have various major impacts on human society through their influence on natural ecosystems, food production and biotic interactions, including diseases. In this study, we used a combination of statistical genetics, experimental evolution and common garden experiments to investigate the evolutionary potential for thermal adaptation in the potato late blight pathogen, Phytophthora infestans, and infer its likely response to changing temperatures. We found a trade‐off associated with thermal adaptation to heterogeneous environments in P. infestans, with the degree of the trade‐off peaking approximately at the pathogen's optimum growth temperature. A genetic trade‐off in thermal adaptation was also evidenced by the negative association between a strain's growth rate and its thermal range for growth, and warm climates selecting for a low pathogen growth rate. We also found a mirror effect of phenotypic plasticity and genetic adaptation on growth rate. At below the optimum, phenotypic plasticity enhances pathogen's growth rate but nature selects for slower growing genotypes when temperature increases. At above the optimum, phenotypic plasticity reduces pathogen's growth rate but natural selection favours for faster growing genotypes when temperature increases further. We conclude from these findings that the growth rate of P. infestans will only be marginally affected by global warming.     

Native jewelweed,but not other native species,displays post‐invasion trait divergence

Invasive exotic plants reduce the diversity of native communities by displacing native species. According to the coexistence theory, native plants are able to coexist with invaders only when their fitness is not significantly smaller than that of the exotics or when they occupy a different niche. It has therefore been hypothesized that the survival of some native species at invaded sites is due to post‐invasion evolutionary changes in fitness and/or niche traits. In common garden experiments, we tested whether plants from invaded sites of two native species, Impatiens noli‐tangere and Galeopsis speciosa, outperform conspecifics from non‐invaded sites when grown in competition with the invader (Impatiens parviflora). We further examined whether the expected superior performance of the plants from the invaded sites is due to changes in the plant size (fitness proxy) and/or changes in the germination phenology and phenotypic plasticity (niche proxies). Invasion history did not influence the performance of any native species when grown with the exotic competitor. In I. noli‐tangere, however, we found significant trait divergence with regard to plant size, germination phenology and phenotypic plasticity. In the absence of a competitor, plants of I. noli‐tangere from invaded sites were larger than plants from non‐invaded sites. The former plants germinated earlier than inexperienced conspecifics or an exotic congener. Invasion experience was also associated with increased phenotypic plasticity and an improved shade‐avoidance syndrome. Although these changes indicate fitness and niche differentiation of I. noli‐tangere at invaded sites, future research should examine more closely the adaptive value of these changes and their genetic basis.     

Evolution of stickleback feeding behaviour: genetics of population divergence at different ontogenetic stages

The evolutionary significance of individual consistency in a given behaviour – called animal personality – has been subject to a lot of recent research. However, the genetic underpinnings of population divergence in mean personality have rarely been studied, especially across different ontogenetic stages. Previous work has shown that marine vs. pond populations of nine‐spined sticklebacks (Pungitius pungitius) have undergone adaptive divergence in a series of fitness‐related traits, including behaviour. One particular behavioural trait important in this system is feeding activity: giant pond sticklebacks are more active feeders than their normal sized marine conspecifics. In a common garden experiment, we raised individuals from pure and hybrid F₁‐generation crosses of a highly divergent marine – pond population pair to see if (i) feeding activity and/or its ontogenetic change was consistent between individuals, and if (ii) population divergence at different ontogenetic stages could be explained by additive genetic, nonadditive genetic or maternal effects. We found that feeding activity decreased with age, but that these changes were consistently different among both individuals and crosses. The among cross patterns were consistent with a nonadditive genetic scenario: in the early period pond sticklebacks expressed dominance for high feeding activity, while in the late period marine sticklebacks expressed dominance for low feeding activity. We conclude that nine‐spined sticklebacks exhibit different feeding personalities, and that the population divergence in feeding personality is explainable by age‐dependent expression of genetic dominance.     

Gene flow does not prevent personality and morphological differentiation between two blue tit populations

Understanding the causes and consequences of population phenotypic divergence is a central goal in ecology and evolution. Phenotypic divergence among populations can result from genetic divergence, phenotypic plasticity or a combination of the two. However, few studies have deciphered these mechanisms for populations geographically close and connected by gene flow, especially in the case of personality traits. In this study, we used a common garden experiment to explore the genetic basis of the phenotypic divergence observed between two blue tit (Cyanistes caeruleus) populations inhabiting contrasting habitats separated by 25 km, for two personality traits (exploration speed and handling aggression), one physiological trait (heart rate during restraint) and two morphological traits (tarsus length and body mass). Blue tit nestlings were removed from their population and raised in a common garden for up to 5 years. We then compared adult phenotypes between the two populations, as well as trait‐specific Q_st and F_st. Our results revealed differences between populations similar to those found in the wild, suggesting a genetic divergence for all traits. Q_st–F_st comparisons revealed that the trait divergences likely result from dissimilar selection patterns rather than from genetic drift. Our study is one of the first to report a Q_st–F_st comparison for personality traits and adds to the growing body of evidence that population genetic divergence is possible at a small scale for a variety of traits including behavioural traits.     

Fine‐grained adaptive divergence in an amphibian: genetic basis of phenotypic divergence and the role of nonrandom gene flow in restricting effective migration among wetlands

Adaptive ecological differentiation among sympatric populations is promoted by environmental heterogeneity, strong local selection and restricted gene flow. High gene flow, on the other hand, is expected to homogenize genetic variation among populations and therefore prevent local adaptation. Understanding how local adaptation can persist at the spatial scale at which gene flow occurs has remained an elusive goal, especially for wild vertebrate populations. Here, we explore the roles of natural selection and nonrandom gene flow (isolation by breeding time and habitat choice) in restricting effective migration among local populations and promoting generalized genetic barriers to neutral gene flow. We examined these processes in a network of 17 breeding ponds of the moor frog Rana arvalis, by combining environmental field data, a common garden experiment and data on variation in neutral microsatellite loci and in a thyroid hormone receptor (TRβ) gene putatively under selection. We illustrate the connection between genotype, phenotype and habitat variation and demonstrate that the strong differences in larval life history traits observed in the common garden experiment can result from adaptation to local pond characteristics. Remarkably, we found that haplotype variation in the TRβ gene contributes to variation in larval development time and growth rate, indicating that polymorphism in the TRβ gene is linked with the phenotypic variation among the environments. Genetic distance in neutral markers was correlated with differences in breeding time and environmental differences among the ponds, but not with geographical distance. These results demonstrate that while our study area did not exceed the scale of gene flow, ecological barriers constrained gene flow among contrasting habitats. Our results highlight the roles of strong selection and nonrandom gene flow created by phenological variation and, possibly, habitat preferences, which together maintain genetic and phenotypic divergence at a fine‐grained spatial scale.     

Parasite‐mediated selection in a natural metapopulation of Daphnia magna

Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, nonadaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a Q_ST–F_ST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.     

Extensive variation,but not local adaptation in an Australian alpine daisy

Alpine plants often occupy diverse habitats within a similar elevation range, but most research on local adaptation in these plants has focused on elevation gradients. In testing for habitat‐related local adaptation, local effects on seed quality and initial plant growth should be considered in designs that encompass multiple populations and habitats. We tested for local adaptation across alpine habitats in a morphologically variable daisy species, Brachyscome decipiens, in the Bogong High Plains in Victoria, Australia. We collected seed from different habitats, controlled for maternal effects through initial seed size estimates, and characterized seedling survival and growth in a field transplant experiment. We found little evidence for local adaptation for survival or plant size, based on three adaptation measures: Home versus Away, Local versus Foreign, and Sympatric versus Allopatric (SA). The SA measure controlled for planting site and population (site‐of‐origin) effects. There were significant differences due to site‐of‐origin and planting site effects. An important confounding factor was the size of plants directly after transplantation of seedlings, which had a large impact on subsequent seedling survival and growth. Initial differences in plant width and height influenced subsequent survival across the growing season but in opposing directions: wide plants had higher survival, but tall plants had lower survival. In an additional controlled garden experiment at Cranbourne Royal Botanic Gardens, site‐of‐origin effects detected in the field experiments disappeared under more benign homogeneous conditions. Although B. decipiens from different source areas varied significantly when grown across a range of alpine habitats, these differences did not translate into a local or habitat‐related fitness advantage. This lack of local advantage may signal weak past selection, and/or weak adaptive transgeneration (plasticity) effects.