Adaptive plasticity and genetic divergence in feeding efficiency during parallel adaptive radiation of whitefish (Coregonus spp.)

Parallel phenotypic divergence in replicated adaptive radiations could either result from parallel genetic divergence in response to similar divergent selection regimes or from equivalent phenotypically plastic response to the repeated occurrence of contrasting environments. In post‐glacial fish, replicated divergence in phenotypes along the benthic‐limnetic habitat axis is commonly observed. Here, we use two benthic‐limnetic species pairs of whitefish from two Swiss lakes, raised in a common garden design, with reciprocal food treatments in one species pair, to experimentally measure whether feeding efficiency on benthic prey has a genetic basis or whether it underlies phenotypic plasticity (or both). To do so, we offered experimental fish mosquito larvae, partially burried in sand, and measured multiple feeding efficiency variables. Our results reveal both, genetic divergence as well as phenotypically plastic divergence in feeding efficiency, with the phenotypically benthic species raised on benthic food being the most efficient forager on benthic prey. This indicates that both, divergent natural selection on genetically heritable traits and adaptive phenotypic plasticity, are likely important mechanisms driving phenotypic divergence in adaptive radiation.     

Genetic variation for sensitivity to a thyme monoterpene in associated plant species

Recent studies have shown that plant allelochemicals can have profound effects on the performance of associated species, such that plants with a history of co-existence with “chemical neighbour” plants perform better in their presence compared to naïve plants. This has cast new light on the complexity of plant–plant interactions and plant communities and has led to debates on whether plant communities are more co-evolved than traditionally thought. In order to determine whether plants may indeed evolve in response to other plants’ allelochemicals it is crucial to determine the presence of genetic variation for performance under the influence of specific allelochemicals and show that natural selection indeed operates on this variation. We studied the effect of the monoterpene carvacrol—a dominant compound in the essential oil of Thymus pulegioides—on three associated plant species originating from sites where thyme is either present or absent. We found the presence of genetic variation in both naïve and experienced populations for performance under the influence of the allelochemical but the response varied among naïve and experienced plant. Plants from experienced populations performed better than naïve plants on carvacrol soil and contained significantly more seed families with an adaptive response to carvacrol than naïve populations. This suggests that the presence of T. pulegioides can act as a selective agent on associated species, by favouring genotypes which perform best in the presence of its allelochemicals. The response to the thyme allelochemical varied from negative to neutral to positive among the species. The different responses within a species suggest that plant–plant interactions can evolve; this has implications for community dynamics and stability.     

Evaluating the influence of life‐history characteristics on genetic structure: a comparison of small mammals inhabiting complex agricultural landscapes

Conversion of formerly continuous native habitats into highly fragmented landscapes can lead to numerous negative demographic and genetic impacts on native taxa that ultimately reduce population viability. In response to concerns over biodiversity loss, numerous investigators have proposed that traits such as body size and ecological specialization influence the sensitivity of species to habitat fragmentation. In this study, we examined how differences in body size and ecological specialization of two rodents (eastern chipmunk; Tamias striatus and white‐footed mouse; Peromyscus leucopus) impact their genetic connectivity within the highly fragmented landscape of the Upper Wabash River Basin (UWB), Indiana, and evaluated whether landscape configuration and complexity influenced patterns of genetic structure similarly between these two species. The more specialized chipmunk exhibited dramatically more genetic structure across the UWB than white‐footed mice, with genetic differentiation being correlated with geographic distance, configuration of intervening habitats, and complexity of forested habitats within sampling sites. In contrast, the generalist white‐footed mouse resembled a panmictic population across the UWB, and no landscape factors were found to influence gene flow. Despite the extensive previous work in abundance and occupancy within the UWB, no landscape factor that influenced occupancy or abundance was correlated with genetic differentiation in either species. The difference in predictors of occupancy, abundance, and gene flow suggests that species‐specific responses to fragmentation are scale dependent.     

Limited gene flow may enhance adaptation to local optima in isolated populations of the Roesel's bush cricket (Metrioptera roeselii)

Variation in morphological traits along latitudinal gradients often manifests as size clines. In insects, both positive and negative correlations are seen, and the mechanism behind the response is unclear. We studied variation in seven morphological traits of Roesel's bush cricket, Metrioptera roeselii, sampled from seven latitude-matched-pair populations that were either geographically isolated from or connected to the species continuous distribution range. The aim was to examine whether morphological traits differed between isolated and continuous populations, and whether latitudinal variation was apparent. The data were used to indicate whether variation in trait means originates from plastic responses to the environment or genetic adaptation to local conditions. To evaluate the influence of gene flow on trait means, we analysed the genetic variation in seven microsatellites. Data showed that individuals from isolated populations display a positive relationship between latitude and body size, whereas individuals from continuous populations show little or no such relationship. The combined morphological and genetic data suggest that the isolated populations have adapted to local optima, while gene flow between continuous populations appears to counteract this process.     

Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation

The expansion of invasive species challenges our understanding of the process of adaptation. Given that the invasion process often entails population bottlenecks, it is surprising that many invasives appear to thrive even with low levels of sequence-based genetic variation. Using Amplified Fragment Length Polymorphism (AFLP) and methylation sensitive-AFLP (MS-AFLP) markers, we tested the hypothesis that differentiation of invasive Japanese knotweed in response to new habitats is more correlated with epigenetic variation than DNA sequence variation. We found that the relatively little genetic variation present was differentiated among species, with less differentiation among sites within species. In contrast, we found a great deal of epigenetic differentiation among sites within each species and evidence that some epigenetic loci may respond to local microhabitat conditions. Our findings indicate that epigenetic effects could contribute to phenotypic variation in genetically depauperate invasive populations. Deciphering whether differences in methylation patterns are the cause or effect of habitat differentiation will require manipulative studies.     

Conflicts in maintaining biodiversity at multiple scales

Biodiversity consists of multiple scales, including functional diversity in ecological traits, species diversity and genetic diversity within species, and is declining across the globe, largely in response to human activities. While species extinctions are the most obvious aspect of this, there has also been a more insidious loss of genetic diversity within species. While a vast literature concerns each of these scales of biodiversity, less is known about how different scales affect one another. In particular, genetic and species diversity may influence each other in numerous ways, both positively and negatively. However, we know little about the mechanism behind these patterns. In this issue of Molecular Ecology, Nestmann et al. (2011) experimentally explore the effect of species and functional diversity and composition of grassland plant communities on the genetic structure of one of the component species. Increasing species richness led to greater changes in the genetic composition of the focal populations over 4 years, primarily because of genetic drift in smaller population sizes. However, there were also genetic changes in response to particular plant functional groups, indicating selective differences driven by plant community composition. These results suggest that different levels of biodiversity can trade-off in communities, which may prove a challenge for conservation biologists seeking to preserve all aspects of biodiversity.     

Rapid eco-evolutionary responses in perturbed phytoplankton communities

Biodiversity currently faces unprecedented threats owing to species extinctions. Ecologically, compensatory dynamics can ensure stable community biomass following perturbation. However, whether there is a contribution of genetic diversity to community responses is an outstanding question. To date, the contribution of evolutionary processes through genotype shifts has not been assessed in naturally co-occurring multi-species communities in the field. We examined the mechanisms contributing to the response of a lake phytoplankton community exposed to either a press or pulse acidification perturbation in lake mesocosms. To assess community shifts in the ecological response of morphospecies, we identified taxa microscopically. We also assessed genotype shifts by sequencing the ITS2 region of ribosomal DNA. We observed ecological and genetic contributions to community responses. The ecological response was attributed to compensatory morphospecies dynamics and occurred primarily in the Pulse perturbation treatment. In the Press treatments, in addition to compensatory dynamics, we observed evidence for genotype selection in two species of chlorophytes, Desmodesmus cuneatus and an unidentified Chlamydomonas. Our study demonstrates that while genotype selection may be rare, it is detectable and occurs especially when new environmental conditions are maintained for long enough to force selection processes on standing variation.     

Plasticity paves the way in an adaptive radiation

Phenotypic plasticity has been hypothesized to play a central role in the evolution of phenotypic diversity across species (West‐Eberhard 2003 ). Through ‘genetic assimilation’, phenotypes that are initially environmentally induced within species become genetically fixed over evolutionary time. While genetic assimilation has been shown to occur in both the laboratory and the field (Waddington 1953 ; Aubret & Shine 2009 ), it remains to be shown whether it can account for broad patterns of phenotypic diversity across entire adaptive radiations. Furthermore, our ignorance of the underlying molecular mechanisms has hampered our ability to incorporate phenotypic plasticity into models of evolutionary processes. In this issue of Molecular Ecology, Parsons et al. ( 2016 ) take a significant step in filling these conceptual gaps making use of cichlid fishes as a powerful study system. Cichlid jaw and skull morphology show adaptive, plastic changes in response to early dietary experiences (Fig. 1). In this research, Parsons et al. ( 2016 ) first show that the direction of phenotypic plasticity aligns with the major axis of phenotypic divergence across species. They then dissect the underlying genetic architecture of this plasticity, showing that it is specific to the developmental environment and implicating the patched locus in genetic assimilation (i.e. a reduction in the environmental sensitivity of that locus in the derived species).     

MC1R-dependent, melanin-based colour polymorphism is associated with cell-mediated response in the Eleonora's falcon

Colour polymorphism in vertebrates is usually under genetic control and may be associated with variation in physiological traits. The melanocortin 1 receptor (Mc1r) has been involved repeatedly in melanin-based pigmentation but it was thought to have few other physiological effects. However, recent pharmacological studies suggest that MC1R could regulate the aspects of immunity. We investigated whether variation at Mc1r underpins plumage colouration in the Eleonora's falcon. We also examined whether nestlings of the different morphs differed in their inflammatory response induced by phytohemagglutinin (PHA). Variation in colouration was due to a deletion of four amino acids at the Mc1r gene. Cellular immune response was morph specific. In males, but not in females, dark nestling mounted a lower PHA response than pale ones. Although correlative, our results raise the neglected possibility that MC1R has pleiotropic effects, suggesting a potential role of immune capacity and pathogen pressure on the maintenance of colour polymorphism in this species.     

Adaptive phenotypic divergence in an annual grass differs across biotic contexts*

Climate is a powerful force shaping adaptation within species, yet adaptation to climate occurs against a biotic background: species interactions can filter fitness consequences of genetic variation by altering phenotypic expression of genotypes. We investigated this process using populations of teosinte, a wild annual grass related to maize (Zea mays ssp. mexicana), sampling plants from 10 sites along an elevational gradient as well as rhizosphere biota from three of those sites. We grew half‐sibling teosinte families in each biota to test whether trait divergence among teosinte populations reflects adaptation or drift, and whether rhizosphere biota affect expression of diverged traits. We further assayed the influence of rhizosphere biota on contemporary additive genetic variation. We found that adaptation across environment shaped divergence of some traits, particularly flowering time and root biomass. We also observed that different rhizosphere biota shifted expressed values of these traits within teosinte populations and families and altered within‐population genetic variance and covariance. In sum, our results imply that changes in trait expression and covariance elicited by rhizosphere communities could have played a historical role in teosinte adaptation to environments and that they are likely to play a role in the response to future selection.     

Species divergence in offspring begging intensity: difference in need or manipulation of parents?

Conflicts over the delivery and sharing of food among family members are expected to lead to evolution of exaggerated offspring begging for food. Coevolution between offspring begging intensity and parent response depends on the genetic architecture of the traits involved. Given a genetic correlation between offspring begging intensity and parental response, there may be fast and arbitrary divergence in these behaviours between populations. However, there is limited knowledge about the genetic basis of offspring solicitation and parental response and whether these traits are genetically correlated. In this study, we performed a partial cross-fostering experiment of young between pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) and recorded the behaviour of individual offspring and their (foster)parents. We found that nestling collared flycatchers reached a higher phenotypic quality, estimated both as mass at fledging and as intensity of their T-lymphocyte-mediated immune response when raised by heterospecific foster parents. However, although collared flycatchers begged relatively more intensively, we found no evidence of corresponding higher resistance (i.e. lower feeding rate) of adult collared flycatchers than of adult pied flycatchers. Thus, the difference in offspring begging intensity between the two species seems not to be a result of a difference in escalation of the parent-offspring conflict. Instead, the species' divergence in exaggeration of offspring begging intensity 'honestly' matches a difference between the species in offspring need. This interpretation is strengthened by the fact that the difference in begging intensity between the two species increased as the season progressed, coinciding with the higher sensitivity of nestling collared flycatchers to the seasonal decline in food availability. Thus, the behavioural differentiation appears to be a direct consequence of a life-history differentiation (offspring growth patterns).     

Phenotypic plasticity allows the Mediterranean parsley frog Pelodytes punctatus to exploit two temporal niches under continuous gene flow

Environmental changes, such as climate change, lead to the opening of new niches. In such situations, species that adapt to new niches can survive and/or expand their ranges. However, gene flow can hamper genetic adaptation to new environments. Alternatively, recent models have highlighted the importance of phenotypic plasticity in tracking environmental change. Here, we investigate whether phenotypic plasticity or genetic evolution (or both) allows an amphibian species to exploit two divergent climatic niches. In the Mediterranean region, the parsley frog Pelodytes punctatus breeds both in spring, as do most other species, and in autumn, a temporal niche not exploited by most other species, but which may become increasingly important with global warming. Conditions of development are dramatically different between the two seasons and deeply impact tadpole life-history traits. To determine whether these temporal niches are exploited by two genetically differentiated subpopulations, or whether the bimodal phenology arises in a panmictic population displaying plastic life-history traits, we use two complementary approaches. We measure both molecular genetic differentiation and quantitative-trait differentiation between spring and autumn cohorts, using microsatellites and common garden experiments, respectively. Seasonal cohorts were not genetically differentiated and differences in tadpole life history between cohorts were not maintained in laboratory conditions. We conclude that phenotypic plasticity, rather than genetic adaptation, allows Parsley frog to exploit two contrasting temporal niches.     

Do females adjust brood sex ratio according to males’ genetic structures in a gregarious passerine,the vinous‐throated parrotbill Paradoxornis webbianus?

A growing number of bird species are known to have fine‐scale genetic structure during the breeding season, with relatives breeding in close vicinity. Such genetic structure often has fitness consequences for parents, and sex ratio theory predicts that females should respond adaptively when they determine offspring sex. We examined whether or not females allocate offspring sex adaptively in response to the local genetic structures as well as other biotic and abiotic factors in a population of the vinous‐throated parrotbill Paradoxornis webbianus, a small passerine with strong flocking habit and various genetic structures among neighbouring males during the breeding season. The average brood sex ratio of hatchlings (secondary sex ratio) did not deviate from parity. In addition, the observed brood sex ratio was independent of the fine‐scale genetic structure and other factors including breeding density, clutch size, laying date, parents’ quality, and the presence of extrapair paternity. Accordingly, we reject the hypothesis of adaptive sex allocation by female parrotbills in association with local genetic structure and other factors. Instead we conclude that despite the plausible benefits of biased sex allocation, this species determines brood sex ratio via random sex allocation with equal probability of male and female offspring.     

A test of genotypic variation in specificity of herbivore-induced responses in Solidago altissima L. (Asteraceae)

Plant-induced responses to multiple herbivores can mediate ecological interactions among herbivore species, thereby influencing herbivore community composition in nature. Several studies have indicated high specificity of induced responses to different herbivore species. In addition, there may be genetic variation for plant response specificity that can have significant ecological implications, by altering the competitive strength and hierarchical relationships among interacting herbivore species. However, few studies have examined whether plant populations harbor genetic variation for induction specificity. Using three distinct genotypes of Solidago altissima plants, we examined whether specialist herbivore species Dichomeris leuconotella, Microrhopala vittata, and Trirhabda virgata elicit specific induction responses from plants (specificity of elicitation), and whether induction differentially affects these herbivore species (specificity of effect). Results from bioassays and secondary metabolite analyses suggest that there is specificity of both elicitation and effect in the induced responses: D. leuconotella and M. vittata preferred and performed better on leaves damaged by conspecifics than heterospecifics, and induced qualitatively different secondary metabolite profiles. In contrast, T. virgata equally avoided but physiologically tolerated all types of damage. These patterns of specificity suggest that plant-induced responses mediate asymmetric competitive interactions between herbivore species, which potentially intensifies inter-specific relative to intra-specific competition. Plant genotypes widely differed in overall susceptibility to the herbivores and secondary metabolite production, yet we found no genotype-by-treatment interactions in insect performance, preference and plant secondary metabolite production. This lack of genetic variation for induction specificity suggests that competitive interactions between herbivore species on S. altissima are homogeneous across plant genotypes.     

Genetic variation in a phylogenetic context: Responses of two specialized leaf beetles (Coleoptera: Chrysomelidae) to host plants of their congeners

This work explores the possibility that constraints on genetic variation guide host shifts and are responsible for the evolutionary conservatism of host affiliation in phytophagous insects. To this end, we used full- and half-sib breeding designs to screen two species of the North American bettle genus Ophraella for genetic variation in larval and adult feeding responses to several host plants of other species of Ophraella. All the plants are in the family Asteraceae. In O. conferta, we observed effectively no feeding response, and hence no genetic variation in response, to three of five test plant species; only those plants related to the species' natural hosts evoked genetically variable responses. In O. artemisiae, adults displayed genetic variation in response to a congener of the natural host, but not to two distantly related plants. However, significant variation among full-sib broods in larval feeding suggests the existence of nonadditive genetic variance in feeding response to all five species of test plants—although survival was very low on most of them. The results suggest that patterns of presence versus apparent absence of detectable genetic variation may be related to the chemical similarity of plants to the insects' natural hosts, but not evidently to the phylogenetic history of host affiliation within the genus. Almost all genetic correlations in responses to host plants were not significantly different from zero; the few significant correlations were positive, and negative correlations that might explain host specificity were not found. Our data do not explain why exclusive shifts to new hosts should occur, but the apparent lack of genetic variation in responses to some plants suggests that the direction of host shifts is genetically constrained.     

Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits?

Aim The southern European peninsulas (Iberian, Italian and Balkan) are considered to have been refugia for many European species of plants and animals during the climatic extremes of the Pleistocene ice ages. A number of recent studies (fossil and genetic), however, have provided evidence for full‐glacial survival of some species beyond these peninsulas. Here we explore the biogeographical traits of these species, and ask whether they possessed certain characteristics that enabled them to persist in more northerly refugia. Location Europe. Methods Fossil and genetic evidence for refugial localities of species that survived in Europe during the last full‐glacial was obtained from the literature (totalling 90 species: 34 woody plants and 56 vertebrates). Forty‐seven of these species (23 woody plants and 24 vertebrates) had fossil evidence, whereas the remaining 43 species (11 woody plants and 32 vertebrates) had only genetic evidence. All species were scored according to their present geographical distribution, habitat preference and life‐history traits. The species were classified on the basis of these traits using hierarchical cluster analysis. Analysis of similarities was used to examine differences in vertebrate and woody plant species groups that survived only in southerly refugia and those that also persisted in more northerly locations. Non‐metric multi‐dimensional scaling was used to examine patterns observed between and within groups. Results Results from our analysis of species with fossil and genetic evidence for survival in refugia reveal that species that survived only in southerly refugia were large‐seeded trees or thermophilous vertebrates. In contrast, species that had a full‐glacial distribution, including more northerly locations, were wind‐dispersed, habitat‐generalist trees with the ability to reproduce vegetatively, and habitat‐generalist mammals with present‐day northerly distributions. Main conclusions Analysis of the geographical distribution, habitat preference and life‐history traits of the species studied suggests that underlying biogeographical traits may have determined their response to Pleistocene glaciation. The traits most commonly found in present populations with a northerly distribution in Europe enabled the same species to exist much farther north than the southern European peninsulas during the full‐glacial. It is possible that many of these species are now in restricted populations, within the ‘warm‐stage’ refugia of the current interglacial. The northerly full‐glacial survival of a number of woody plants and vertebrate species has significant implications for understanding migration rates of these species in response to climate change. It also has important implications for understanding current patterns of genetic diversity of European species. We suggest that both fossil and genetic evidence should be used to identify and prioritize for conservation of refugial localities in southern and northern Europe.     

Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species

Most quantitative traits are thought to exhibit high levels of genetic variance and evolutionary potential. However, this conclusion may be biased by a lack of studies on nonmodel organisms and may not generalize to restricted species. A recent study on a single, southern population of the rainforest-restricted Drosophila birchii failed to find significant additive genetic variance for the desiccation resistance trait; however, it is unclear whether this pattern extends to other D. birchii populations or to other rainforest species. Here we use an animal model design to show very low levels of additive genetic variance for desiccation resistance in multiple populations of two highly sensitive rainforest species of Drosophila from tropical northeastern Australia. In contrast, relatively high levels of genetic variance were found for morphological traits in all populations of the species tested. This indicates limited evolutionary potential for evolving increased desiccation resistance in these rainforest restricted species.     

Effects of species traits on the genetic diversity of high-mountain plants: a multi-species study across the Alps and the Carpathians

Aim  To test the influence of various species traits, elevation and phylogeographical history on the genetic diversity of high-mountain plants in the Alps and Carpathians.
Location  The regular sampling grid comprised the whole range of the European Alps and the Carpathians.
Methods  Twenty-two high-mountain plant species were exhaustively sampled and their genetic diversity was assessed with amplified fragment length polymorphisms (AFLPs). ANOVAs were used to check for relationships between species traits and species genetic diversity, and to test whether genetic diversity was influenced by altitude and phylogeographical history (i.e. Alps versus Carpathians).
Results  In both mountain systems, species dispersed and pollinated by wind showed higher genetic diversity than species with self or insect pollination, and with animal- or gravity-dispersed seeds. Only in the Alps did altitudinal range size affect species genetic diversity significantly: species with narrow altitudinal ranges in the highest vegetation belts had significantly higher genetic diversity than those expanding over wide altitudinal ranges. Genetic diversity was species specific and significantly higher in the Alps than in the Carpathians, but it was not influenced by elevation.
Main conclusions  Wind pollination and wind dispersal seem to foster high genetic diversity. However, species traits are often associated and their effects on genetic diversity cannot be clearly disentangled. As genetic diversity is species specific, comparisons across species need to be interpreted with care. Genetic diversity was generally lower in the Carpathians than in the Alps, due to higher topographical isolation of alpine habitats in the Carpathians and this mountain massif's divergent phylogeographical history. Elevation did not influence genetic diversity, challenging the long-held view of decreasing genetic diversity with increasing elevation in mountain plants.     

Ambulatory dispersal in <Emphasis Type="Italic">Tetranychus urticae</Emphasis>: an artificial selection experiment on propensity to disperse yields no response

Dispersal to new hosts is an important process for an invasive herbivore, such as the two-spotted spider mite. A recent study, using artificial selection experiments, has suggested that genetic variation and genetic trade-offs are present for propensity to disperse in this species. However, due to the experimental setup alternative explanations for the response to selection could not be ruled out. Using an altered setup, we investigated whether the propensity for ambulatory dispersal differs genetically between individuals and whether genetic correlations with life-history traits exist. Upward and downward selection on propensity to leave the colony was performed for seven generations in four replicate artificial selection experiments and the results were compared to control lines. No consistent responses to selection were found and no significant effect on life-history traits (oviposition rate, juvenile survival, development rate and number of adult offspring) or sex ratio was present across the replicates. The data suggest that our base population of spider mites harbours at best a low amount of additive genetic variation for this behaviour.