Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish

Coral reefs are highly diverse ecosystems, where numerous closely related species often coexist. How new species arise and are maintained in these high geneflow environments have been long‐standing conundrums. Hybridization and patterns of introgression between sympatric species provide a unique insight into the mechanisms of speciation and the maintenance of species boundaries. In this study, we investigate the extent of hybridization between two closely related species of coral reef fish: the common coral trout (Plectropomus leopardus) and the bar‐cheek coral trout (Plectropomus maculatus). Using a complementary set of 25 microsatellite loci, we distinguish pure genotype classes from first‐ and later‐generation hybrids, identifying 124 interspecific hybrids from a collection of 2,991 coral trout sampled in inshore and mid‐shelf reefs of the southern Great Barrier Reef. Hybrids were ubiquitous among reefs, fertile and spanned multiple generations suggesting both ecological and evolutionary processes are acting to maintain species barriers. We elaborate on these finding to investigate the extent of genomic introgression and admixture from 2,271 SNP loci recovered from a ddRAD library of pure and hybrid individuals. An analysis of genomic clines on recovered loci indicates that 261 SNP loci deviate from a model of neutral introgression, of which 132 indicate a pattern of introgression consistent with selection favouring both hybrid and parental genotypes. Our findings indicate genome‐wide, bidirectional introgression between two sympatric species of coral reef fishes and provide further support to a growing body of evidence for the role of hybridization in the evolution of coral reef fishes.     

Population genomics and the causes of local differentiation

Exactly 50 years ago, a revolution in empirical population genetics began with the introduction of methods for detecting allelic variation using protein electrophoresis (Throckmorton 1962; Hubby 1963; Lewontin & Hubby 1966). These pioneering scientists showed that populations are chock‐full of genetic variation. This variation was a surprise that required a re‐thinking of evolutionary genetic heuristics. Understanding the causes for the maintenance of this variation became and remains a major area of research. In the process of addressing the causes, this same group of scientists documented geographical genetic structure (Prakash et al. 1969), spawning the continued accumulation of what is now a huge case study catalogue of geographical differentiation (e.g. Loveless & Hamrick 1984; Linhart & Grant 1996). Geographical differentiation is clearly quite common. Yet, a truly general understanding of the patterns in and causes of spatial genetic structure across the genome remains elusive. To what extent is spatial structure driven by drift and phylogeography vs. geographical differences in environmental sources of selection? What proportion of the genome participates? A general understanding requires range‐wide data on spatial patterning of variation across the entire genome. In this issue of Molecular Ecology, Lasky et al. (2012) make important strides towards addressing these issues, taking advantage of three contemporary revolutions in evolutionary biology. Two are technological: high‐throughput sequencing and burgeoning computational power. One is cultural: open access to data from the community of scientists and especially data sets that result from large collaborative efforts. Together, these developments may at last put answers within reach.     

Into the wild—WAMBAM goes to Canada

The sixth Wild Animal Models Bi‐Annual Meeting was held in July 2017 in Québec, with 42 participants. This report documents the evolution of questions asked and approaches used in evolutionary quantitative genetic studies of wild populations in recent decades, and how these questions and approaches were represented at the recent meeting. We explore how ideas from previous meetings in this series have developed to their present states, and consider how the format of the meetings may be particularly useful at fostering the rapid development and proliferation of ideas and approaches.     

The Park Grass Experiment and next‐generation approaches: local adaptation of sweet vernal grass revisited

Long‐term ecological experiments provide unique opportunities to observe the effects of natural selection. The Park Grass Experiment at Rothamsted Experiment Station in Hertfordshire, UK, is the longest running ecological experiment that incorporates fertilization treatments and has been ongoing since 1856. In the 1970s, local adaptation was observed in the grass Anthoxanthum odoratum to the elevated soil aluminium levels of the fertilized plots. Gould et al. ( 2014 ) have utilized this system to reevaluate the extent of local adaptation, first documented nearly 45 years ago (Snaydon 1970 ), and to use emerging molecular approaches to identify candidate genes for the adaptation. From their work, they identify several plausible candidate loci for aluminium tolerance. This work shows the power of long‐term field‐based trials in a scientific age concentrated on rapidly emerging molecular techniques often utilized in short, narrowly focused laboratory or controlled environment experiments. The current study clearly illustrates the benefits gained by combining these molecular approaches within long‐term monitoring experiments that can be regularly revisited in a changing world and used to address questions on evolutionary scales.     

Landscape genomics and a common garden trial reveal adaptive differentiation to temperature across Europe in the tree species Alnus glutinosa

The adaptive potential of tree species to cope with climate change has important ecological and economic implications. Many temperate tree species experience a wide range of environmental conditions, suggesting high adaptability to new environmental conditions. We investigated adaptation to regional climate in the drought‐sensitive tree species Alnus glutinosa (Black alder), using a complementary approach that integrates genomic, phenotypic and landscape data. A total of 24 European populations were studied in a common garden and through landscape genomic approaches. Genotyping‐by‐sequencing was used to identify SNPs across the genome, resulting in 1990 SNPs. Although a relatively low percentage of putative adaptive SNPs was detected (2.86% outlier SNPs), we observed clear associations among outlier allele frequencies, temperature and plant traits. In line with the typical drought avoiding nature of A. glutinosa, leaf size varied according to a temperature gradient and significant associations with multiple outlier loci were observed, corroborating the ecological relevance of the observed outlier SNPs. Moreover, the lack of isolation by distance, the very low genetic differentiation among populations and the high intrapopulation genetic variation all support the notion that high gene exchange combined with strong environmental selection promotes adaptation to environmental cues.     

Genomic evidence for parallel adaptation to cities

Urban evolutionary biology is the study of rapid evolutionary change in response to humans and our uses of land to support city dwellers. Because cities are relatively modern additions to the natural world, research on urban evolution tends to focus on microevolutionary change that has happened across a few to many hundreds of generations. These questions still fall under the broad purview of evolutionary ecology. However, the severity, rapidity and replication of environmental changes that drive evolution in this context make it worthy of specific attention. Urban evolution provides the opportunity to study the earliest stages of evolution in a context that is scientifically interesting and societally important. The newness of urban populations and their proximity to natural populations also creates challenges when trying to detect population genetic change. In a From the Cover article in this issue of Molecular Ecology, Mueller et al. use whole genome resequencing data to address some of these challenges while exploring genetic changes associated with urbanization in three replicate urban‐rural burrowing owl (Athene cunicularia) populations. Combining multiple approaches across these sample sites Mueller et al. find evidence for selection on genes whose function is related to synapses, neuron projections, brain connectivity and cognitive function in general. That selection was parallel suggests that phenotypes related to brain processes were probably particularly important for urban adaptation.     

Integration of Random Forest with population‐based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha)

Anadromous Chinook salmon populations vary in the period of river entry at the initiation of adult freshwater migration, facilitating optimal arrival at natal spawning. Run timing is a polygenic trait that shows evidence of rapid parallel evolution in some lineages, signifying a key role for this phenotype in the ecological divergence between populations. Studying the genetic basis of local adaptation in quantitative traits is often impractical in wild populations. Therefore, we used a novel approach, Random Forest, to detect markers linked to run timing across 14 populations from contrasting environments in the Columbia River and Puget Sound, USA. The approach permits detection of loci of small effect on the phenotype. Divergence between populations at these loci was then examined using both principle component analysis and F_ST outlier analyses, to determine whether shared genetic changes resulted in similar phenotypes across different lineages. Sequencing of 9107 RAD markers in 414 individuals identified 33 predictor loci explaining 79.2% of trait variance. Discriminant analysis of principal components of the predictors revealed both shared and unique evolutionary pathways in the trait across different lineages, characterized by minor allele frequency changes. However, genome mapping of predictor loci also identified positional overlap with two genomic outlier regions, consistent with selection on loci of large effect. Therefore, the results suggest selective sweeps on few loci and minor changes in loci that were detected by this study. Use of a polygenic framework has provided initial insight into how divergence in a trait has occurred in the wild.     

Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana

Selection on quantitative trait loci (QTL) may vary among natural environments due to differences in the genetic architecture of traits, environment‐specific allelic effects or changes in the direction and magnitude of selection on specific traits. To dissect the environmental differences in selection on life history QTL across climatic regions, we grew a panel of interconnected recombinant inbred lines (RILs) of Arabidopsis thaliana in four field sites across its native European range. For each environment, we mapped QTL for growth, reproductive timing and development. Several QTL were pleiotropic across environments, three colocalizing with known functional polymorphisms in flowering time genes (CRY2, FRI and MAF2‐5), but major QTL differed across field sites, showing conditional neutrality. We used structural equation models to trace selection paths from QTL to lifetime fitness in each environment. Only three QTL directly affected fruit number, measuring fitness. Most QTL had an indirect effect on fitness through their effect on bolting time or leaf length. Influence of life history traits on fitness differed dramatically across sites, resulting in different patterns of selection on reproductive timing and underlying QTL. In two oceanic field sites with high prereproductive mortality, QTL alleles contributing to early reproduction resulted in greater fruit production, conferring selective advantage, whereas alleles contributing to later reproduction resulted in larger size and higher fitness in a continental site. This demonstrates how environmental variation leads to change in both QTL effect sizes and direction of selection on traits, justifying the persistence of allelic polymorphism at life history QTL across the species range.     

The danger of applying the breeder's equation in observational studies of natural populations

The breeder's equation, which predicts evolutionary change when a phenotypic covariance exists between a heritable trait and fitness, has provided a key conceptual framework for studies of adaptive microevolution in nature. However, its application requires strong assumptions to be made about the causation of fitness variation. In its univariate form, the breeder's equation assumes that the trait of interest is not correlated with other traits having causal effects on fitness. In its multivariate form, the validity of predicted change rests on the assumption that all such correlated traits have been measured and incorporated into the analysis. Here, we (i) highlight why these assumptions are likely to be seriously violated in studies of natural, rather than artificial, selection and (ii) advocate wider use of the Robertson–Price identity as a more robust, and less assumption‐laden, alternative to the breeder's equation for applications in evolutionary ecology.     

Heterozygote advantage at MHC DRB may influence response to infectious disease epizootics

The effect of MHC polymorphism on individual fitness variation in the wild remains equivocal; however, much evidence suggests that heterozygote advantage is a major determinant. To understand the contribution of MHC polymorphism to individual disease resistance or susceptibility in natural populations, we investigated two MHC class II B loci, DQB and DRB, in the New Zealand sea lion (NZSL, Phocarctos hookeri). The NZSL is a threatened species which is unusually susceptible to death by bacterial infection at an early age; it has suffered three bacterial induced epizootics resulting in high mortality levels of young pups since 1997. The MHC DQB and DRB haplotypes of dead NZSL pups with known cause of death (bacteria, enteritis or trauma) were sequenced and reconstructed, compared to pups that survived beyond 2 months of age, and distinct MHC DRB allele frequency and genotype differences were identified. Two findings were striking: (i) one DRB allele was present only in dead pups, and (ii) one heterozygous DRB genotype, common in live pups, was absent from dead pups. These results are consistent with some functional relationship with these variants and suggest heterozygote advantage is operating at DRB. We found no association between heterozygosity and fitness at 17 microsatellite loci, indicating that general heterozygosity is not responsible for the effect on fitness detected here. This result may be a consequence of recurrent selection by multiple pathogen assault over recent years and highlights the importance of heterozygote advantage at MHC as a potential mechanism for fitness differences in wild populations.     

Genome‐wide signature of local adaptation linked to variable CpG methylation in oak populations

It has long been known that adaptive evolution can occur through genetic mutations in DNA sequence, but it is unclear whether adaptive evolution can occur through analogous epigenetic mechanisms, such as through DNA methylation. If epigenetic variation contributes directly to evolution, species under threat of disease, invasive competition, climate change or other stresses would have greater stores of variation from which to draw. We looked for evidence of natural selection acting on variably methylated DNA sites using population genomic analysis across three climatologically distinct populations of valley oaks. We found patterns of genetic and epigenetic differentiations that indicate local adaptation is operating on large portions of the oak genome. While CHG methyl polymorphisms are not playing a significant role and would make poor targets for natural selection, our findings suggest that CpG methyl polymorphisms as a whole are involved in local adaptation, either directly or through linkage to regions under selection.     

Somatic mutations as a useful tool for studying clonal dynamics in trees

The seemingly eternal cycles of clonal growth in many tree species, with members of Populus (aspen, poplars, cottonwoods and the like) featuring most prominently, provoke a number of questions on the interface between ecology, genetics and forestry. In this issue, two groups present their approaches to clonal dynamics ( Ally et al. 2008 and Mock et al. 2008 ), using microsatellite (or simple sequence repeat, SSR) variation in P. tremuloides. Ally et al. developed and applied a model for using microsatellites to estimate clone age and infer other community characteristics. Mock et al. used fewer microsatellites but in more individuals, to examine clone size and distribution across the landscape.     

Rapid adaptation to climate change

In recent years, amid growing concerns that changing climate is affecting species distributions and ecosystems, predicting responses to rapid environmental change has become a major goal. In this issue, Franks and colleagues take a first step towards this objective (Franks et al. 2016). They examine genomewide signatures of selection in populations of Brassica rapa after a severe multiyear drought. Together with other authors, Franks had previously shown that flowering time was reduced after this particular drought and that the reduction was genetically encoded. Now, the authors have sequenced previously stored samples to compare allele frequencies before and after the drought and identify the loci with the most extreme shifts in frequencies. The loci they identify largely differ between populations, suggesting that different genetic variants may be responsible for reduction in flowering time in the two populations.     

The genetic consequences of selection in natural populations

The selection coefficient, s, quantifies the strength of selection acting on a genetic variant. Despite this parameter's central importance to population genetic models, until recently we have known relatively little about the value of s in natural populations. With the development of molecular genetic techniques in the late 20th century and the sequencing technologies that followed, biologists are now able to identify genetic variants and directly relate them to organismal fitness. We reviewed the literature for published estimates of natural selection acting at the genetic level and found over 3000 estimates of selection coefficients from 79 studies. Selection coefficients were roughly exponentially distributed, suggesting that the impact of selection at the genetic level is generally weak but can occasionally be quite strong. We used both nonparametric statistics and formal random‐effects meta‐analysis to determine how selection varies across biological and methodological categories. Selection was stronger when measured over shorter timescales, with the mean magnitude of s greatest for studies that measured selection within a single generation. Our analyses found conflicting trends when considering how selection varies with the genetic scale (e.g., SNPs or haplotypes) at which it is measured, suggesting a need for further research. Besides these quantitative conclusions, we highlight key issues in the calculation, interpretation, and reporting of selection coefficients and provide recommendations for future research.     

Using the Mus musculus hybrid zone to assess covariation and genetic architecture of limb bone lengths

Two subspecies of the house mouse, Mus musculus domesticus and Mus musculus musculus, meet in a narrow contact zone across Europe. Mice in the hybrid zone are highly admixed, representing the full range of mixed ancestry from the two subspecies. Given the distinct morphologies of these subspecies, these natural hybrids can be used for genomewide association mapping at sufficiently high resolution to directly infer candidate genes. We focus here on limb bone length differences, which is of special interest for understanding the evolution of developmentally correlated traits. We used 172 first‐generation descendants of wild‐caught mice from the hybrid zone to measure the length of stylopod (humerus/femur), zeugopod (ulna/tibia) and autopod (metacarpal/metatarsal) elements in skeletal CT scans. We find phenotypic covariation between limb elements in the hybrids similar to patterns previously described in Mus musculus domesticus inbred strains, suggesting that the hybrid genotypes do not influence the covariation pattern in a major way. Mapping was performed using 143,592 SNPs and identified several genomic regions associated with length differences in each bone. Bone length was found to be highly polygenic. None of the candidate regions include the canonical genes known to control embryonic limb development. Instead, we are able to identify candidate genes with known roles in osteoblast differentiation and bone structure determination, as well as recently evolved genes of, as yet, unknown function.     

Beyond splitting hares and rabbiting on about major histocompatibility complex complexity

The genes of the major histocompatibility complex (MHC) have become the target of choice for studies wishing to examine adaptively important genetic diversity in natural populations. Within Molecular Ecology alone, there have been 71 papers on aspects of MHC evolution over the past few years, with an increasing year on year trend. This focus on the MHC is partly driven by the hypothesized links between MHC gene dynamics and ecologically interesting and relevant traits, such as mate choice and host–parasite interactions. However, an ability to pin down the evolutionary causes and ecological consequences of MHC variation in natural populations has proven challenging and has been hampered by the very issue that is attractive about MHC genes – their high levels of diversity. Linking high levels of MHC diversity to ecological factors in inherently complex natural populations requires a level of experimental design and analytical rigour that is extremely difficult to achieve owing to a plethora of potentially confounding and interacting variables. In this issue of Molecular Ecology, Smith et al. (2010) elegantly overcome the challenge of detecting complex interactions in complex systems by using an intricate analytical approach to demonstrate a role for MHC in the reproductive ability of a natural population of the European hare Lepus europaeus ( Fig. 1 ). Also in this issue, Oppelt et al. (2010) demonstrate a role for MHC variation in determining levels of hepatic coccidian infection in the European rabbit Oryctolagus cuniculus ( Fig. 2 ).

Figure 1 Open in figure viewer PowerPoint The European hare (Lepus europaeus).     

The genomic and physiological basis of life history variation in a butterfly metapopulation

Unravelling the mechanisms underlying variation in life history traits is of fundamental importance for our understanding of adaptation by natural selection. While progress has been made in mapping fitness-related phenotypes to genotypes, mainly in a handful of model organisms, functional genomic studies of life history adaptations are still in their infancy. In particular, despite a few notable exceptions, the genomic basis of life history variation in natural populations remains poorly understood. This is especially true for the genetic underpinnings of life history phenotypes subject to diversifying selection driven by ecological dynamics in patchy environments--as opposed to adaptations involving strong directional selection owing to major environmental changes, such as latitudinal gradients, extreme climatic events or transitions from salt to freshwater. In this issue of Molecular Ecology,Wheat et al. (2011) now make a significant leap forward by applying the tools of functional genomics to dispersal-related life history variation in a butterfly metapopulation. Using a combination of microarrays, quantitative PCR and physiological measurements, the authors uncover several metabolic and endocrine factors that likely contribute to the observed life history phenotypes. By identifying molecular candidate mechanisms of fitness variation maintained by dispersal dynamics in a heterogeneous environment,they also begin to address fascinating interactions between the levels of physiology, ecology and evolution.     

Genome‐wide evidence for divergent selection between populations of a major agricultural pathogen

The genetic and environmental homogeneity in agricultural ecosystems is thought to impose strong and uniform selection pressures. However, the impact of this selection on plant pathogen genomes remains largely unknown. We aimed to identify the proportion of the genome and the specific gene functions under positive selection in populations of the fungal wheat pathogen Zymoseptoria tritici. First, we performed genome scans in four field populations that were sampled from different continents and on distinct wheat cultivars to test which genomic regions are under recent selection. Based on extended haplotype homozygosity and composite likelihood ratio tests, we identified 384 and 81 selective sweeps affecting 4% and 0.5% of the 35 Mb core genome, respectively. We found differences both in the number and the position of selective sweeps across the genome between populations. Using a XtX‐based outlier detection approach, we identified 51 extremely divergent genomic regions between the allopatric populations, suggesting that divergent selection led to locally adapted pathogen populations. We performed an outlier detection analysis between two sympatric populations infecting two different wheat cultivars to identify evidence for host‐driven selection. Selective sweep regions harboured genes that are likely to play a role in successfully establishing host infections. We also identified secondary metabolite gene clusters and an enrichment in genes encoding transporter and protein localization functions. The latter gene functions mediate responses to environmental stress, including interactions with the host. The distinct gene functions under selection indicate that both local host genotypes and abiotic factors contributed to local adaptation.     

Genomic and phenotypic differentiation of Arabidopsis thaliana along altitudinal gradients in the North Italian Alps

Altitudinal gradients in mountain regions are short‐range clines of different environmental parameters such as temperature or radiation. We investigated genomic and phenotypic signatures of adaptation to such gradients in five Arabidopsis thaliana populations from the North Italian Alps that originated from 580 to 2350 m altitude by resequencing pools of 19–29 individuals from each population. The sample includes two pairs of low‐ and high‐altitude populations from two different valleys. High‐altitude populations showed a lower nucleotide diversity and negative Tajima's D values and were more closely related to each other than to low‐altitude populations from the same valley. Despite their close geographic proximity, demographic analysis revealed that low‐ and high‐altitude populations split between 260 000 and 15 000 years before present. Single nucleotide polymorphisms whose allele frequencies were highly differentiated between low‐ and high‐altitude populations identified genomic regions of up to 50 kb length where patterns of genetic diversity are consistent with signatures of local selective sweeps. These regions harbour multiple genes involved in stress response. Variation among populations in two putative adaptive phenotypic traits, frost tolerance and response to light/UV stress was not correlated with altitude. Taken together, the spatial distribution of genetic diversity reflects a potentially adaptive differentiation between low‐ and high‐altitude populations, whereas the phenotypic differentiation in the two traits investigated does not. It may resemble an interaction between adaptation to the local microhabitat and demographic history influenced by historical glaciation cycles, recent seed dispersal and genetic drift in local populations.