The role of genetic constraints on the diversification of Iberian taxa of the genus Aquilegia (Ranunculaceae)

The microevolutionary process of adaptive phenotypic differentiation of quantitative traits between populations or closely‐related taxa depends on the response of populations to the action of natural selection. However, this response can be constrained by the structure of the matrix of additive genetic variance and covariance between traits in each population ( G matrix). In the present study, we obtained additive genetic variance and narrow sense heritability for 25 floral and vegetative traits of three subspecies of Aquilegia vulgaris, and one subspecies of Aquilegia pyrenaica through a common garden crossing experiment. For two vegetative and one floral trait, we also obtained the G matrix and genetic correlations between traits in each subspecies. The amount of genetic variation available in wild populations is not responsible for the larger differentiation of vegetative than floral traits found in this group of columbines. However, the low heritability of some traits constrained their evolution because phenotypic variability among taxa was larger for traits with larger heritability. We confirmed that the process of diversification of the studied taxa involved shifts in the G matrix, mainly determined by changes in the genetic covariance between floral and vegetative traits, probably caused by linkage disequilibrium in narrow endemic taxa. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 252–261.     

Rapid genome‐wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools

There is increasing evidence that evolution can occur rapidly in response to selection. Recent advances in sequencing suggest the possibility of documenting genetic changes as they occur in populations, thus uncovering the genetic basis of evolution, particularly if samples are available from both before and after selection. Here, we had a unique opportunity to directly assess genetic changes in natural populations following an evolutionary response to a fluctuation in climate. We analysed genome‐wide differences between ancestors and descendants of natural populations of Brassica rapa plants from two locations that rapidly evolved changes in multiple phenotypic traits, including flowering time, following a multiyear late‐season drought in California. These ancestor‐descendant comparisons revealed evolutionary shifts in allele frequencies in many genes. Some genes showing evolutionary shifts have functions related to drought stress and flowering time, consistent with an adaptive response to selection. Loci differentiated between ancestors and descendants (F_ST outliers) were generally different from those showing signatures of selection based on site frequency spectrum analysis (Tajima's D), indicating that the loci that evolved in response to the recent drought and those under historical selection were generally distinct. Very few genes showed similar evolutionary responses between two geographically distinct populations, suggesting independent genetic trajectories of evolution yielding parallel phenotypic changes. The results show that selection can result in rapid genome‐wide evolutionary shifts in allele frequencies in natural populations, and highlight the usefulness of combining resurrection experiments in natural populations with genomics for studying the genetic basis of adaptive evolution.     

Genetic variation in flowering phenology and reproductive performance in a Mediterranean high‐mountain specialist,Armeria caespitosa (Plumbaginaceae)

Adaptive responses to past climate change may play an important role in the persistence of high‐mountain plants, which are vulnerable to global warming. Armeria caespitosa is a high‐mountain plant, endemic to the Iberian Central Range. Differences in abiotic environment along the elevational gradient impose two opposing stress gradients (i.e. water stress and duration of the growth season) on the species. Furthermore, the species is found in two interspersed, contrasting microhabitats (rocky outcrops and dry cryophilic grasslands) that have different effects on plants depending of the elevation. As a result of this, the species shows great among‐population variation in many reproductive and vegetative traits. We used a common garden approach to determine whether this phenotypic variation has a genetic basis or is the result of plastic responses shaped by heterogeneous environmental conditions. Plants from the high‐elevation edge and dry cryophilic grasslands flowered earlier and produced more viable fruits but were smaller. These results confirm that among‐population variation in flowering phenology and reproductive performance traits in A. caespitosa is partially genetically based. The results also show that the stronger selection response in favour of early‐flowering individuals in populations at the low‐elevation edge did not correspond with the greater proportion of early‐flowering individuals. Genetic variability associated with flowering onset may be relevant in coping with the impacts of ongoing global warming. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 384–395.     

Small‐scale spatial variation in evolvability for life‐history traits in the storm petrel

The evolutionary potential in the timing of recruitment and reproduction may be crucial for the ability of populations to buffer against environmental changes, allowing them to avoid unfavourable breeding conditions. The evolution of a trait in a local population is determined by its heritability and selection. In the present study, we performed pedigree‐based quantitative genetic analyses for two life‐history traits (recruiting age and laying date) using population data of the storm petrel over an 18‐year period in two adjacent breeding colonies (only 150 m apart) that share the same environmental conditions. In both traits, natal colony effect was the main source of the phenotypic variation among individuals, and cohort variance for recruitment age and additive genetic variance for laying date were natal colony‐specific. We found significant heritability only in laying date and, more specifically, only in birds born in one of the colonies. The difference in genetic variance between the colonies was statistically significant. Interestingly, selection on earlier breeding birds was detected only in the colony in which heritable variation in laying date was found. Therefore, local evolvability for a life‐history trait may vary within a unexpectedly small spatial scale, through the diversifying natural selection and insulating gene flow. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 439–446.     

Phenotypic evolution of an Atlantic Forest passerine (Xiphorhynchus fuscus): biogeographic and systematic implications

We studied the phenotypic variation of the Atlantic Forest passerine Xiphorhynchus fuscus (Aves: Dendrocolaptidae) with the broad aim of addressing whether the history and type of forest affected the evolution of endemic taxa. We also tested whether the different subspecies and genetic lineages of X. fuscus could be considered full species. We collected plumage and body size measurements and, in combination with genetic data, used multivariate tests to evaluate the working hypotheses. Our results, combined with previous biogeographic analyses, indicate that vicariant events have been important determinants in the evolution of phenotypic characters of X. fuscus, once genetic isolation was complete. Our analysis also suggests that forest heterogeneity and ecotones are important factors in the early evolution of Atlantic Forest taxa, perhaps via divergent selection. Forest instability during the Pleistocene was critical in the evolution of phenotypic traits. We confirm that the subspecies atlanticus should be considered a full species. Other lineages or populations are also phenotypically differentiated but we do not suggest considering them as full species. They share high levels of gene flow and are part of a continuous latitudinal cline of phenotypic variation. Our study suggests that not all the historic events in the Atlantic Forest that affected the evolution of genetic lineages also influenced the evolution of phenotypic characters in the same direction and intensity. Undoubtedly, natural selection played a major role in the evolution of Atlantic Forest organisms. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1047–1066.     

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.     

Effects of genetics and light environment on colour expression in threespine sticklebacks

The genetic basis of traits that are under sexual selection and that are involved in recognizing conspecific mates is poorly known, even in systems in which the phenotypic basis of these traits has been well studied. In the present study, we investigate genetic and environmental influences on nuptial colour, which plays important roles in sexual selection and sexual isolation in species pairs of limnetic and benthic threespine sticklebacks ( Gasterosteus aculeatus species complex). Previous work demonstrated that colour differences among species correlate to differences in the ambient light prevalent in their mating habitat. Red fish are found in clear water and black fish in red-shifted habitats. We used a paternal half-sib split-clutch design to investigate the genetic and environmental basis of nuptial colour. We found genetic differences between a red and a black stickleback population in the expression of both red and black nuptial colour. In addition, the light environment influenced colour expression, and genotype by environment interactions were also present. We found evidence for both phenotypic and genetic correlations between our colour traits; some of these correlations are in opposite directions for our red and black populations. These results suggest that both genetic change and phenotypic plasticity underlie the correlation of male colour with light environment.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 663–673.     

Detecting and managing fisheries-induced evolution

Exploitation of fish populations can induce evolutionary responses in life histories. For example, fisheries targeting large individuals are expected to select for early maturation at smaller sizes, leading to reduced fecundity and thus also reduced fisheries yield. These predicted phenotypic shifts have been observed in several fish stocks, but disentangling the environmental and genetic causes behind them has proved difficult. Here, we review recent studies investigating phenotypic shifts in exploited populations and strategies for minimizing fisheries-induced evolution. Responses to selective harvesting will depend on species-specific life-history traits, and on community-level and environmental processes. Therefore, the detection of fisheries-induced evolution and successful fish stock management requires routine population monitoring, and a good understanding of genetics, relevant ecological processes and changing environmental conditions.     

Testing for biases in selection on avian reproductive traits and partitioning direct and indirect selection using quantitative genetic models

Key life history traits such as breeding time and clutch size are frequently both heritable and under directional selection, yet many studies fail to document microevolutionary responses. One general explanation is that selection estimates are biased by the omission of correlated traits that have causal effects on fitness, but few valid tests of this exist. Here, we show, using a quantitative genetic framework and six decades of life‐history data on two free‐living populations of great tits Parus major, that selection estimates for egg‐laying date and clutch size are relatively unbiased. Predicted responses to selection based on the Robertson–Price Identity were similar to those based on the multivariate breeder's equation (MVBE), indicating that unmeasured covarying traits were not missing from the analysis. Changing patterns of phenotypic selection on these traits (for laying date, linked to climate change) therefore reflect changing selection on breeding values, and genetic constraints appear not to limit their independent evolution. Quantitative genetic analysis of correlational data from pedigreed populations can be a valuable complement to experimental approaches to help identify whether apparent associations between traits and fitness are biased by missing traits, and to parse the roles of direct versus indirect selection across a range of environments.     

The contributions of evolutionary divergence and phenotypic plasticity to geographic variation in the western fence lizard,Sceloporus occidentalis

Local genetic adaptation and phenotypic plasticity are two mechanisms that can have marked effects on the morphology, performance, and behaviour of animals, producing geographic variation among populations. However, few studies have examined how these mechanisms interact during ontogeny to shape organismal phenotypes. We incubated eggs of the western fence lizard, Sceloporus occidentalis, from four populations (representing two latitudes and altitudes) in either a warm or cool environment in the laboratory. We then raised the hatchlings under common laboratory conditions, measured morphological and performance traits until 5 weeks of age, and compared juvenile morphology with that of field‐caught adults from each population. The results obtained indicate that some phenotypic traits that contribute to performance (body size, hindlimb length, head shape) were relatively canalized in juveniles and differed among populations in a way that was consistent with adults from their population of origin. However, other traits (forelimb length, inter‐limb length, mass, tail length), showed significant effects of incubation temperature, and this environmentally induced variation persisted throughout the experiment. Although selection pressure may be stronger for traits that are integral to survival, developmental effects might still have a lasting impact on traits less important to organismal fitness. We discuss the results obtained in the present study the context of the life history of these animals. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 84–98.     

Calls,colours, shape,and genes: a multi‐trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis

Evolutionary divergence in behavioural traits related to mating may represent the initial stage of speciation. Direct selective forces are usually invoked to explain divergence in mate‐recognition traits, often neglecting a role for neutral processes or concomitant differentiation in ecological traits. We adopted a multi‐trait approach to obtain a deeper understanding of the mechanisms behind allopatric divergence in the Amazonian frog, Allobates femoralis. We tested the null hypothesis that geographic distance between populations correlates with genetic and phenotypic divergence, and compared divergence between mate‐recognition (acoustic) and ecological (coloration, body‐shape) traits. We quantified geographic variation in 39 phenotypic traits and a mitochondrial DNA marker among 125 individuals representing eight populations. Geographic variation in acoustic traits was pronounced and tracked the spatial genetic variation, which appeared to be neutral. Thus, the evolution of acoustic traits tracked the shared history of the populations, which is unexpected for pan‐Amazonian taxa or for mate‐recognition traits. Divergence in coloration appeared uncorrelated with genetic distance, and might be partly attributed to local selective pressures, and perhaps to Batesian mimicry. Divergence in body‐shape traits was low. The results obtained depict a complex evolutionary scenario and emphasize the importance of considering multiple traits when disentangling the forces behind allopatric divergence. ©2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 826–838.     

Phenotypic integration between antipredator behavior and camouflage pattern in juvenile sticklebacks

Predation is a strong selective force that promotes the evolution of antipredator behaviors and camouflage in prey animals. However, the independent evolution of single traits cannot explain how observed phenotypic variations of these traits are maintained within populations. We studied genetic and phenotypic correlations between antipredator behaviors (shoaling and risk‐taking) and morphology traits (pigmentation and size) in juvenile three‐spined sticklebacks by using pedigree‐based quantitative genetic analysis to test phenotypic integration (or complex phenotype) as an evolutionary response to predation risk. Individuals with strongly melanized (i.e., camouflaged) phenotype and genotype were less sociable to conspecifics, but bolder during foraging under predation risk. Individuals with faster growing phenotype and genotype were bolder, and those with lager eyes were more fearful. These phenotypic integrations were not confounded with correlated plastic responses to predation risk because the phenotypes were measured in naïve fish born in the laboratory, but originated from a natural population with predation pressure. Consistent selection for particular combinations of traits under predation pressure or pleiotropic genes might influence the maintenance of the genetic (co)variations and polymorphism in melanin color, growth trajectory, and behavior patterns.     

Naturally occurring variation in tadpole morphology and performance linked to predator regime

Divergent natural selection drives a considerable amount of the phenotypic and genetic variation observed in natural populations. For example, variation in the predator community can generate conflicting selection on behavioral, life‐history, morphological, and performance traits. Differences in predator regime can subsequently increase phenotypic and genetic variations in the population and result in the evolution of reproductive barriers (ecological speciation) or phenotypic plasticity. We evaluated morphology and swimming performance in field collected Bronze Frog larvae (Lithobates clamitans) in ponds dominated by predatory fish and those dominated by invertebrate predators. Based on previous experimental findings, we hypothesized that tadpoles from fish‐dominated ponds would have small bodies, long tails, and large tail muscles and that these features would facilitate fast‐start speed. We also expected to see increased tail fin depth (i.e., the tail‐lure morphology) in tadpoles from invertebrate‐dominated ponds. Our results support our expectations with respect to morphology in affecting swimming performance of tadpoles in fish‐dominated ponds. Furthermore, it is likely that divergent natural selection is playing a role in the diversification on morphology and locomotor performance in this system.     

Morphological anti‐predator defences in the nine‐spined stickleback: constitutive,induced or both?

Environmental differences among populations are expected to lead to local adaptation, while spatial or temporal environmental variation within a population will favour evolution of phenotypic plasticity. As plasticity itself can be under selection, locally adapted populations can vary in levels of plasticity. Nine‐spined stickleback (Pungitius pungitius) originating from isolated ponds (low piscine predation risk, high competition) vs. lake and marine populations (high piscine predation risk, low competition) are known to be morphologically adapted to their respective environments. However, nothing is known about their ability to express phenotypic plasticity in morphology in response to perceived predation risk or food availability/competition. We studied predator‐induced phenotypic plasticity in body shape and armour of marine and pond nine‐spined stickleback in a factorial common garden experiment with two predator treatments (present vs. absent) and two feeding regimes (low vs. high). The predation treatment did not induce any morphological shifts in fish from either habitat or food regime. However, strong habitat‐dependent differences between populations as well as strong sexual dimorphism in both body shape and armour were found. The lack of predator‐induced plasticity in development of the defence traits (viz. body armour and body depth) suggests that morphological anti‐predator traits in nine‐spined stickleback are strictly constitutive, rather than inducible. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Rapid evolution of thermal plasticity in mountain lake Daphnia populations

Populations at risk of extinction due to climate change may be rescued by adaptive evolution or plasticity. Selective agents, such as introduced predators, may enhance or constrain plastic or adaptive responses to temperature. We tested responses of Daphnia to temperature by collecting populations from lakes across an elevational gradient in the presence and absence of fish predators (long‐term selection). We subsequently grew these populations at two elevations in field mesocosms over two years (short‐term selection), followed by a common‐garden experiment at two temperatures in the lab to measure life‐history traits. Both long‐term and short‐term selection affected traits, suggesting that genetic variation of plasticity within populations enabled individuals to rapidly evolve plasticity in response to high temperature. We found that short‐term selection by high temperature increased plasticity for growth rate in all populations. Fecundity was higher in populations from fishless lakes and body size showed greater plasticity in populations from warm lakes (long‐term selection). Neither body size nor fecundity were affected by short‐term thermal selection. These results demonstrate that plasticity is an important component of the life‐history response of Daphnia, and that genetic variation within populations enabled rapid evolution of plasticity in response to selection by temperature.     

Diversifying selection drives parallel evolution of gill raker number and body size along the speciation continuum of European whitefish

Adaptive radiation is the evolution of ecological and phenotypical diversity. It arises via ecological opportunity that promotes the exploration of underutilized or novel niches mediating specialization and reproductive isolation. The assumed precondition for rapid local adaptation is diversifying natural selection, but random genetic drift could also be a major driver of this process. We used 27 populations of European whitefish (Coregonus lavaretus) from nine lakes distributed in three neighboring subarctic watercourses in northern Fennoscandia as a model to test the importance of random drift versus diversifying natural selection for parallel evolution of adaptive phenotypic traits. We contrasted variation for two key adaptive phenotypic traits correlated with resource utilization of polymorphic fish; the number of gill rakers and the total length of fish, with the posterior distribution of neutral genetic differentiation from 13 microsatellite loci, to test whether the observed phenotypic divergence could be achieved by random genetic drift alone. Our results show that both traits have been under diversifying selection and that the evolution of these morphs has been driven by isolation through habitat adaptations. We conclude that diversifying selection acting on gill raker number and body size has played a significant role in the ongoing adaptive radiation of European whitefish morphs in this region.     

Evidence for long‐term change in length,mass and migration phenology of anadromous spawners in French Atlantic salmon Salmo salar

This study provides new data on Atlantic salmon Salmo salar life‐history traits across France. Using a long‐term recreational angling database (1987–2013) covering 34 rivers in three regions (genetic units), a decline in individual length, mass and a delayed adult return to French rivers was reported. Temporal similarities in trait variations between regions may be attributed to common change in environmental conditions at sea. The relative rate of change in phenotypic traits was more pronounced in early maturing fish [1 sea‐winter (1SW) fish] than in late maturing fish (2SW fish). Such contrasted response within populations highlights the need to account for the diversity in life histories when exploring mechanisms of phenotypic change in S. salar. Such detailed life‐history data on returning S. salar have not previously been reported from France. This study on French populations also contributes to reducing the gap in knowledge by providing further empirical evidence of a global pattern in S. salar across its distribution range. Results are consistent with the hypothesis that the observed changes in life‐history traits are primarily associated with environmental changes in the North Atlantic Ocean. They also emphasize the presence of less important, but still significant contrasts between region and life history.     

QUANTIFYING EVOLUTIONARY POTENTIAL OF MARINE FISH LARVAE: HERITABILITY,SELECTION, AND EVOLUTIONARY CONSTRAINTS

For many marine fish, intense larval mortality may provide considerable opportunity for selection, yet much less is known about the evolutionary potential of larval traits. We combined field demographic studies and manipulative experiments to estimate quantitative genetic parameters for both larval size and swimming performance for a natural population of a common coral‐reef fish, the bicolor damselfish (Stegastes partitus). We also examined selection on larval size by synthesizing information from published estimates of selective mortality. We introduce a method that uses the Lande–Arnold framework for examining selection on quantitative traits to empirically reconstruct adaptive landscapes. This method allows the relationship between phenotypic value and fitness components to be described across a broad range of trait values. Our results suggested that despite strong viability selection for large larvae and moderate heritability (h²= 0.29), evolutionary responses of larvae would likely be balanced by reproductive selection favoring mothers that produce more, smaller offspring. Although long‐term evolutionary responses of larval traits may be constrained by size‐number trade‐offs, our results suggest that phenotypic variation in larval size may be an ecologically important source of variability in population dynamics through effects on larval survival and recruitment to benthic populations.     

Genetic and morphologic diversity of European fan palm (Chamaerops humilis L.) populations from different environments from Sicily

Chamaerops humilis is decreasing in abundance in Mediterranean Europe, which has induced the European community to call for its protection in Special Areas of Conservation. However, information about its genetic and morphological variability, which is crucial to the development of any conservation strategies, is insufficient. The present study aimed to investigate the genetic and morphological variability of C. humilis in Sicily, which was selected as a model because of the high number of dense populations. The relationships between morphological traits and climatic variables were studied to highlight patterns of adaptation to the environment, along with the genetic similarity among the populations. Ten natural populations were sampled, analyzed using 28 specifically designed SSR primers, and evaluated based on 29 morphological traits. The populations were clustered similarly based on genetic and morphological traits. Heterozygosity was high and inbreeding coefficients were low. These results, along with higher intra‐ than inter‐population differentiation, suggest that C. humilis populations in Sicily differentiated from a common ancestor and that inter‐population variation arose from secondary evolution processes induced by ecological adaptation. The correlations between climatic variables and morphological traits suggest that the morphological adaptation to arid environments depends more on summer temperatures than on evapotranspiration or rainfall and that autumn and winter temperatures are determinants of the species establishment at new sites. Considering the response of C. humilis to seasonal temperatures, the present results indicate this species as a candidate for tracking climatic changes in Europe. Further studies are needed to highlight the adaptation of C. humilis to cold environments. Palaeo‐climatological and ‐ecological studies could help clarify its strategies for the colonization of new sites. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 66–81.     

Rapid,broad‐scale gene expression evolution in experimentally harvested fish populations

Gene expression changes potentially play an important role in adaptive evolution under human‐induced selection pressures, but this has been challenging to demonstrate in natural populations. Fishing exhibits strong selection pressure against large body size, thus potentially inducing evolutionary changes in life history and other traits that may be slowly reversible once fishing ceases. However, there is a lack of convincing examples regarding the speed and magnitude of fisheries‐induced evolution, and thus, the relevant underlying molecular‐level effects remain elusive. We use wild‐origin zebrafish (Danio rerio) as a model for harvest‐induced evolution. We experimentally demonstrate broad‐scale gene expression changes induced by just five generations of size‐selective harvesting, and limited genetic convergence following the cessation of harvesting. We also demonstrate significant allele frequency changes in genes that were differentially expressed after five generations of size‐selective harvesting. We further show that nine generations of captive breeding induced substantial gene expression changes in control stocks likely due to inadvertent selection in the captive environment. The large extent and rapid pace of the gene expression changes caused by both harvest‐induced selection and captive breeding emphasizes the need for evolutionary enlightened management towards sustainable fisheries.