Genetic rescue: a safe or risky bet?

Small and isolated populations face threats from genetic drift and inbreeding. To rescue populations from these threats, conservation biologists can augment gene flow into small populations to increase variation and reduce inbreeding depression. Spectacular success stories include greater prairie chickens in Illinois (Westermeier et al. 1998 ), adders in Sweden (Madsen et al. 1999 ) and panthers in Florida (Johnson et al. 2010 ). However, we also know that performing such crosses risks introducing genes that may be poorly adapted to local conditions or genetic backgrounds. A classic example of such ‘outbreeding depression’ occurred when different subspecies of ibex from Turkey and the Sinai were introduced to assist recovery of an ibex population in Czechoslovakia (Templeton 1986 ). Despite being fertile, the hybrids birthed calves too early, causing the whole population to disappear. In the face of uncertainty, conservation biologists have tended to respect genetic identity, shying away from routinely crossing populations. In this issue of Molecular Ecology, Frankham ( 2015 ) compiles empirical data from experimental studies to assess the costs and benefits of between‐population crosses (Fig.  1 ). Crosses screened to exclude those involving highly divergent populations or distinct habitats show large heterosis with few apparent risks of outbreeding depression. This leads Frankham to advocate for using assisted gene flow more widely. But do the studies analysed in this meta‐analysis adequately test for latent outcrossing depression?     

Genome architecture enables local adaptation of Atlantic cod despite high connectivity

Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large ~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation.     

Tracing the recombination and colonization history of hybrid species in space and time

Hybrid speciation has long fascinated evolutionary biologists and laymen alike, presumably because it challenges our classical view of evolution as a ‘one‐way street’ leading to strictly tree‐like patterns of ancestry and descent. Homoploid hybrid speciation (HHS) has been a particularly interesting puzzle, as it appears to occur extremely rapidly, perhaps within less than 50 generations ( McCarthy et al. 1995 ; Buerkle et al. 2000 ). Nevertheless, HHS may sometimes involve extended or repeated periods of recombination and gene exchange between populations subject to strong divergent natural selection ( Buerkle & Rieseberg 2008 ). Thus, HHS provides a highly interesting setting for understanding the drivers and tempo of adaptive divergence and speciation in the face of gene flow ( Arnold 2006 ; Rieseberg & Willis 2007 ; Nolte & Tautz 2009). In the present issue of Molecular Ecology, Wang et al. (2011) explore a particularly challenging issue connected to HHS: they attempt to trace the colonization and recombination history of an ancient (several MYA) hybrid species, from admixture and recombination in the ancestral hybrid zone to subsequent range shifts triggered by tectonic events (uplift of the Tibetan plateau) and climatic shifts (Pleistocene ice ages). This work is important because it addresses key issues related to the origin of the standing genetic variation available for adaptive responses (e.g. to climate change) and speciation in temperate species, which are topics of great current interest ( Rieseberg et al. 2003 ; Barrett & Schluter 2008 ; de Carvalho et al. 2010 ).     

Pathogen pollution and the emergence of a deadly amphibian pathogen

Imagine a single pathogen that is responsible for mass mortality of over a third of an entire vertebrate class. For example, if a single pathogen were causing the death, decline and extinction of 30% of mammal species (including humans), the entire world would be paying attention. This is what has been happening to the world's amphibians – the frogs, toads and salamanders that are affected by the chytrid fungal pathogen, Batrachochytrium dendrobatidis (referred to as Bd), which are consequently declining at an alarming rate. It has aptly been described as the worst pathogen in history in terms of its effects on biodiversity (Kilpatrick et al. 2010). The pathogen was only formally described about 13 years ago (Longcore et al. 1999), and scientists are still in the process of determining where it came from and investigating the question: why now? Healthy debate has ensued as to whether Bd is a globally endemic organism that only recently started causing high mortality due to shifting host responses and/or environmental change (e.g. Pounds et al. 2006) or whether a virulent strain of the pathogen has rapidly disseminated around the world in recent decades, affecting new regions with a vengeance (e.g. Morehouse et al. 2003; Weldon et al. 2004; Lips et al. 2008). We are finally beginning to shed more light on this question, due to significant discoveries that have emerged as a result of intensive DNA‐sequencing methods comparing Bd isolates from different amphibian species across the globe. Evidence is mounting that there is indeed a global panzootic lineage of Bd (BdGPL) in addition to what appear to be more localized endemic strains (Fisher et al. 2009; James et al. 2009; Farrer et al. 2011). Additionally, BdGPL appears to be a hypervirulent strain that has resulted from the hybridization of different Bd strains that came into contact in recent decades, and is now potentially replacing the less‐virulent endemic strains of the pathogen (Farrer et al. 2011). In a new study published in this issue of Molecular Ecology, Schloegel et al. (2012) identify an additional unique Bd lineage that is endemic to the Atlantic Brazilian rainforests (Bd‐Brazil) and provide striking evidence that the Bd‐Brazil lineage has sexually recombined with the BdGPL lineage in an area where the two lineages likely came into contact as a result of classic anthropogenically mediated ‘pathogen pollution’(see below). Fungal pathogens, including Bd, have the propensity to form recombinant lineages when allopatric populations that have not yet formed genetic reproductive barriers are provided with opportunities to intermingle, and virulent strains may be selected for because they tend to be highly transmissible (Fisher et al. 2012). As Schloegel et al. (2012) point out, the demonstrated ability for Bd to undergo meiosis may also mean that it has the capacity to form a resistant spore stage (as yet undiscovered), based on extrapolation from other sexually reproducing chytrids that all have spore stages.     

Go forth,evolve and prosper: the genetic basis of adaptive evolution in an invasive species

Invasive species stand accused of a familiar litany of offences, including displacing native species, disrupting ecological processes and causing billions of dollars in ecological damage (Cox 1999 ). Despite these transgressions, invasive species have at least one redeeming virtue – they offer us an unparalleled opportunity to investigate colonization and responses of populations to novel conditions in the invaded habitat (Elton 1958 ; Sakai et al. 2001 ). Invasive species are by definition colonists that have arrived and thrived in a new location. How they are able to thrive is of great interest, especially considering a paradox of invasion (Sax & Brown 2000 ): if many populations are locally adapted (Leimu & Fischer 2008 ), how could species introduced into new locations become so successful? One possibility is that populations adjust to the new conditions through plasticity – increasing production of allelopathic compounds (novel weapons), or taking advantage of new prey, for example. Alternatively, evolution could play a role, with the populations adapting to the novel conditions of the new habitat. There is increasing evidence, based on phenotypic data, for rapid adaptive evolution in invasive species (Franks et al. 2012 ; Colautti & Barrett 2013 ; Sultan et al. 2013 ). Prior studies have also demonstrated genetic changes in introduced populations using neutral markers, which generally do not provide information on adaptation. Thus, the genetic basis of adaptive evolution in invasive species has largely remained unknown. In this issue of Molecular Ecology, Vandepitte et al. ( 2014 ) provide some of the first evidence in invasive populations for molecular genetic changes directly linked to adaptation.     

Phenotypic plasticity and divergence in gene expression

The extent to which phenotypic plasticity, or the ability of a single genotype to produce different phenotypes in different environments, impedes or promotes genetic divergence has been a matter of debate within evolutionary biology for many decades (see, for example, Ghalambor et al. 2007 ; Pfennig et al. 2010 ). Similarly, the role of evolution in shaping phenotypic plasticity remains poorly understood (Pigliucci 2005 ). In this issue of Molecular Ecology, Dayan et al. ( 2015 ) provide empirical data relevant to these questions by assessing the extent of plasticity and divergence in the expression levels of 2272 genes in muscle tissue from killifish (genus Fundulus) exposed to different temperatures. F. heteroclitus (Fig.  1 A) and F. grandis are minnows that inhabit estuarine marshes (Fig.  1 B) along the coasts of the Atlantic Ocean and Gulf of Mexico in North America. These habitats undergo large variations in temperature both daily and seasonally, and these fish are known to demonstrate substantial phenotypic plasticity in response to temperature change (e.g. Fangue et al. 2006 ). Furthermore, the range of F. heteroclitus spans a large latitudinal gradient of temperatures, such that northern populations experience temperatures that are on average ~10°C colder than do southern populations (Schulte 2007 ). By comparing gene expression patterns between populations of these fish from different thermal habitats held in the laboratory at three different temperatures, Dayan et al. ( 2015 ) address two important questions regarding the interacting effects of plasticity and evolution: (i) How does phenotypic plasticity affect adaptive divergence? and (ii) How does adaptive divergence affect plasticity?     

Ring species as demonstrations of the continuum of species formation

In the mid‐20th century, Ernst Mayr (1942) and Theodosius Dobzhansky (1958) championed the significance of ‘circular overlaps’ or ‘ring species’ as the perfect demonstration of the gradual nature of species formation. As an ancestral species expands its range, wrapping around a geographic barrier, derived taxa within the ring display interactions typical of populations, such as genetic and morphological intergradation, while overlapping taxa at the terminus of the ring behave largely as sympatric, reproductively isolated species. Are ring species extremely rare or are they just difficult to detect? What conditions favour their formation? Modelling studies have attempted to address these knowledge gaps by estimating the biological parameters that result in stable ring species (Martins et al. 2013), and determining the necessary topographic parameters of the barriers encircled (Monahan et al. 2012). However, any generalization is undermined by a major limitation: only a handful of ring species are known to exist in nature. In addition, many of them have been broken into multiple species presumed to be evolving independently, usually obscuring the evolutionary dynamics that generate diversity. A paper in this issue of Molecular Ecology by Fuchs et al. (2015), focused on the entire genealogy of a bulbul (Alophoixus) species complex, offers key insights into the evolutionary processes underlying diversification of this Indo‐Malayan bird. Their findings fulfil most of the criteria that can be expected for ring species (Fig.  1 ): an ancestor has colonized the mainland from Sundaland, expanded along the forested habitat wrapping around Thailand's lowlands, adjacent taxa intergrade around the ring distribution, and terminal taxa overlap at the ring closure. Although it remains unclear whether ring divergence has resulted in restrictive gene flow relative to that observed around the ring, their results suggest that circular overlaps might be more common in nature than currently recognized in the literature. Most importantly, this work shows that the continuum of species formation that Mayr and Dobzhansky praised in circular overlaps is found in biological systems currently described as ‘rings of species’, in addition to the idealized ‘ring species’.     

Next‐generation QTL mapping: crowdsourcing SNPs,without pedigrees

For many molecular ecologists, the mantra and mission of the field of ecological genomics could be encapsulated by the phrase ‘to find the genes that matter’ (Mitchell‐Olds 2001 ; Rockman 2012 ). This phrase of course refers to the early hope and current increasing success in the search for genes whose variation underlies phenotypic variation and fitness in natural populations. In the years since the modern incarnation of the field of ecological genomics, many would agree that the low‐hanging fruit has, at least in principle, been plucked: we now have several elegant examples of genes whose variation influences key adaptive traits in natural populations, and these examples have revealed important insights into the architecture of adaptive variation (Hoekstra et al. 2006 ; Shapiro et al. 2009 ; Chan et al. 2010 ). But how well will these early examples, often involving single genes of large effect on discrete or near‐discrete phenotypes, represent the dynamics of adaptive change for the totality of phenotypes in nature? Will traits exhibiting continuous rather than discrete variation in natural populations have as simple a genetic basis as these early examples suggest (Prasad et al. 2012 ; Rockman 2012 )? Two papers in this issue (Robinson et al. 2013 ; Santure et al. 2013 ) not only suggest answers to these questions but also provide useful extensions of statistical approaches for ecological geneticists to study the genetics of continuous variation in nature. Together these papers, by the same research groups studying evolution in a natural population of Great Tits (Parus major), provide a glimpse of what we should expect as the field begins to dissect the genetic basis of what is arguably the most common type of variation in nature, and how genome‐wide surveys of variation can be applied to natural populations without pedigrees.     

Genomics of clinal variation in Drosophila: disentangling the interactions of selection and demography

Clines in phenotypes and genotype frequencies across environmental gradients are commonly taken as evidence for spatially varying selection. Classical examples include the latitudinal clines in various species of Drosophila, which often occur in parallel fashion on multiple continents. Today, genomewide analysis of such clinal systems provides a fantastic opportunity for unravelling the genetics of adaptation, yet major challenges remain. A well‐known but often neglected problem is that demographic processes can also generate clinality, independent of or coincident with selection. A closely related issue is how to identify true genic targets of clinal selection. In this issue of Molecular Ecology, three studies illustrate these challenges and how they might be met. Bergland et al. report evidence suggesting that the well‐known parallel latitudinal clines in North American and Australian D. melanogaster are confounded by admixture from Africa and Europe, highlighting the importance of distinguishing demographic from adaptive clines. In a companion study, Machado et al. provide the first genomic comparison of latitudinal differentiation in D. melanogaster and its sister species D. simulans. While D. simulans is less clinal than D. melanogaster, a significant fraction of clinal genes is shared between both species, suggesting the existence of convergent adaptation to clinaly varying selection pressures. Finally, by drawing on several independent sources of evidence, Bo?i?evi? et al. identify a functional network of eight clinal genes that are likely involved in cold adaptation. Together, these studies remind us that clinality does not necessarily imply selection and that separating adaptive signal from demographic noise requires great effort and care.     

Origins of endemic island tortoises in the western Indian Ocean: a critique of the human‐translocation hypothesis

How do organisms arrive on isolated islands, and how do insular evolutionary radiations arise? In a recent paper, Wilmé et al. ( 2016a ) argue that early Austronesians that colonized Madagascar from Southeast Asia translocated giant tortoises to islands in the western Indian Ocean. In the Mascarene Islands, moreover, the human‐translocated tortoises then evolved and radiated in an endemic genus (Cylindraspis). Their proposal ignores the broad, established understanding of the processes leading to the formation of native island biotas, including endemic radiations. We find Wilmé et al.'s suggestion poorly conceived, using a flawed methodology and missing two critical pieces of information: the timing and the specifics of proposed translocations. In response, we here summarize the arguments that could be used to defend the natural origin not only of Indian Ocean giant tortoises but also of scores of insular endemic radiations world‐wide. Reinforcing a generalist's objection, the phylogenetic and ecological data on giant tortoises, and current knowledge of environmental and palaeogeographical history of the Indian Ocean, make Wilmé et al.'s argument even more unlikely.     

Hybridization between pollination syndromes as an ecological and evolutionary resource

In plants, pollination syndromes (the correlated presence of many features of relevance to pollination mode, for instance pollination by a particular animal clade) are a striking feature of plant biodiversity, providing great floral phenotypic diversity (Fenster et al. 2004 ). Adaptation to a particular animal pollinator provides an explanation for why recently diverged plants can have such extreme differentiation in floral form. One might expect such elaborate adaptations to provide a high degree of pollinator specificity and hence reproductive isolation, but there are many cases where substantial gene flow exists between extreme floral morphs (see Table 1), and the resulting hybrids may be highly fertile. This gene flow provides tremendous opportunities to study the genetics and biology of the pollination syndromes by providing intermediate forms and segregating genotypes. If it is true that pollination syndromes result from adaptation under strong selection, we will expect such flowers to be crucibles of natural selection. If strong selection for particular floral phenotypes can be shown, then this, when coupled with hybridization, will give us one of the most valuable of all experimental systems for evolutionary research: gene flow and selection in balance. In this issue of Molecular Ecology, the paper of Milano et al. ( 2016 ) delivers this. It shows that in populations of the Ipomopsis aggregata complex, gene flow between pollination morphs is high and selection to stabilize those morphs is also high: a probable case of gene flow–selection balance.     

CHROMOSOMAL REARRANGEMENTS AND THE GENETICS OF REPRODUCTIVE BARRIERS IN MIMULUS (MONKEY FLOWERS)

Chromosomal rearrangements may directly cause hybrid sterility and can facilitate speciation by preserving local adaptation in the face of gene flow. We used comparative linkage mapping with shared gene‐based markers to identify potential chromosomal rearrangements between the sister monkeyflowers Mimulus lewisii and Mimulus cardinalis, which are textbook examples of ecological speciation. We then remapped quantitative trait loci (QTLs) for floral traits and flowering time (premating isolation) and hybrid sterility (postzygotic isolation). We identified three major regions of recombination suppression in the M. lewisii × M. cardinalis hybrid map compared to a relatively collinear Mimulus parishii × M. lewisii map, consistent with a reciprocal translocation and two inversions specific to M. cardinalis. These inferences were supported by targeted intraspecific mapping, which also implied a M. lewisii‐specific reciprocal translocation causing chromosomal pseudo‐linkage in both hybrid mapping populations. Floral QTLs mapped in this study, along with previously mapped adaptive QTLs, were clustered in putatively rearranged regions. All QTLs for male sterility, including two underdominant loci, mapped to regions of recombination suppression. We argue that chromosomal rearrangements may have played an important role in generating and consolidating barriers to gene flow as natural selection drove the dramatic ecological and morphological divergence of these species.     

Two adjacent inversions maintain genomic differentiation between migratory and stationary ecotypes of Atlantic cod

Atlantic cod is composed of multiple migratory and stationary populations widely distributed in the North Atlantic Ocean. The Northeast Arctic cod (NEAC) population in the Barents Sea undertakes annual spawning migrations to the northern Norwegian coast. Although spawning occurs sympatrically with the stationary Norwegian coastal cod (NCC), phenotypic and genetic differences between NEAC and NCC are maintained. In this study, we resolve the enigma by revealing the mechanisms underlying these differences. Extended linkage disequilibrium (LD) and population divergence were demonstrated in a 17.4‐Mb region on linkage group 1 (LG1) based on genotypes of 494 SNPs from 192 parents of farmed families of NEAC, NCC or NEACxNCC crosses. Linkage analyses revealed two adjacent inversions within this region that repress meiotic recombination in NEACxNCC crosses. We identified a NEAC‐specific haplotype consisting of 186 SNPs that was fixed in NEAC sampled from the Barents Sea, but segregating under Hardy–Weinberg equilibrium in eight NCC stocks. Comparative genomic analyses determine the NEAC configuration of the inversions to be the derived state and date it to ~1.6–2.0 Mya. The haplotype block harbours 763 genes, including candidates regulating swim bladder pressure, haem synthesis and skeletal muscle organization conferring adaptation to long‐distance migrations and vertical movements down to large depths. Our results suggest that the migratory ecotype experiences strong directional selection for the two adjacent inversions on LG1. Despite interbreeding between NEAC and NCC, the inversions are maintaining genetic differentiation, and we hypothesize the co‐occurrence of multiple adaptive alleles forming a ‘supergene’ in the NEAC population.     

Is variable connectivity among populations of a continental gobiid fish driven by local adaptation or passive dispersal?

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Adaptation despite gene flow? Low recombination helps

About 15,000 years earlier, the Northern half of Europe and North America was buried under a few kilometres of ice. Since then, many organisms have colonized and rapidly adapted to the new, vacant habitats. Some, like the threespine stickleback fish, have done so more successfully than others: from the sea, stickleback have adapted to a multitude of lake and stream habitats with a vast array of complex phenotypes and life histories. Previous studies showed that most of these “ecotypes” differ in multiple divergently selected genes throughout the genome. But how are well‐adapted ecotypes of one habitat protected from maladaptive gene flow from ecotypes of another, adjacent habitat? According to a From the Cover meta‐analysis in this issue of Molecular Ecology (Samuk et al., 2017), low recombination rate regions in the genome offer such protection. While inversions have often been highlighted as an efficient way to maintain linkage disequilibrium among sets of adaptive variants in the face of gene flow, Samuk et al. (2017) show that variation in recombination rate across the genome may perform a similar role in threespine stickleback. With this study, theoretical predictions for the importance of low recombination regions in adaptation are for the first time tested with a highly replicated population genomic data set. The findings from this study have implications for the adaptability of species, speciation and the evolution of genome architecture.     

Simulation modelling in landscape genetics: on the need to go further

With the emergence of landscape genetics, the basic assumptions and predictions of classical population genetic theories are being re‐evaluated to account for more complex spatial and temporal dynamics. Within the last decade, there has been an exponential increase in such landscape genetic studies ( Holderegger & Wagner 2006 ; Storfer et al. 2010 ), and both methodology and underlying concepts of the field are under rapid and constant development. A number of major innovations and a high level of originality are required to fully merge existing population genetic theory with landscape ecology and to develop novel statistical approaches for measuring and predicting genetic patterns. The importance of simulation studies for this specific research has been emphasized in a number of recent articles (e.g., Balkenhol et al. 2009a ; Epperson et al. 2010 ). Indeed, many of the major questions in landscape genetics require the development and application of sophisticated simulation tools to explore gene flow, genetic drift, mutation and natural selection in landscapes with a wide range of spatial and temporal complexities. In this issue, Jaquiéry et al. (2011) provide an excellent example of such a simulation study for landscape genetics. Using a metapopulation simulation design and a novel ‘scale of phenomena’ approach, Jaquiéry et al. (2011) demonstrate the utility and limitations of genetic distances for inferring landscape effects on effective dispersal.     

A hot topic: the genetics of adaptation to geothermal vents in Mimulus guttatus

Identifying the individual loci and mutations that underlie adaptation to extreme environments has long been a goal of evolutionary biology. However, finding the genes that underlie adaptive traits is difficult for several reasons. First, because many traits and genes evolve simultaneously as populations diverge, it is difficult to disentangle adaptation from neutral demographic processes. Second, finding the individual loci involved in any trait is challenging given the respective limitations of quantitative and population genetic methods. In this issue of Molecular Ecology, Hendrick et al. (2016) overcome these difficulties and determine the genetic basis of microgeographic adaptation between geothermal vent and nonthermal populations of Mimulus guttatus in Yellowstone National Park. The authors accomplish this by combining population and quantitative genetic techniques, a powerful, but labour‐intensive, strategy for identifying individual causative adaptive loci that few studies have used (Stinchcombe & Hoekstra 2008 ). In a previous common garden experiment (Lekberg et al. 2012), thermal M. guttatus populations were found to differ from their closely related nonthermal neighbours in various adaptive phenotypes including trichome density. Hendrick et al. (2016) combine quantitative trait loci (QTL) mapping, population genomic scans for selection and admixture mapping to identify a single genetic locus underlying differences in trichome density between thermal and nonthermal M. guttatus. The candidate gene, R2R3 MYB, is homologous to genes involved in trichome development across flowering plants. The major trichome QTL, Tr14, is also involved in trichome density differences in an independent M. guttatus population comparison (Holeski et al. 2010) making this an example of parallel genetic evolution.     

Fission and fusion in island taxa – serendipity,or something to be expected?

A well‐used metaphor for oceanic islands is that they act as ‘natural laboratories’ for the study of evolution. But how can islands or archipelagos be considered analogues of laboratories for understanding the evolutionary process itself? It is not necessarily the case that just because two or more related species occur on an island or archipelago, somehow, this can help us understand more about their evolutionary history. But in some cases, it can. In this issue of Molecular Ecology, Garrick et al. ( 2014 ) use population‐level sampling within closely related taxa of Galapagos giant tortoises to reveal a complex demographic history of the species Chelonoidis becki – a species endemic to Isabela Island, and geographically restricted to Wolf Volcano. Using microsatellite genotyping and mitochondrial DNA sequencing, they provide a strong case for C. becki being derived from C. darwini from the neighbouring island of Santiago. But the interest here is that colonization did not happen only once. Garrick et al. ( 2014 ) reveal C. becki to be the product of a double colonization event, and their data reveal these two founding lineages to be now fusing back into one. Their results are compelling and add to a limited literature describing the evolutionary consequences of double colonization events. Here, we look at the broader implications of the findings of Garrick et al. ( 2014 ) and suggest genomic admixture among multiple founding populations may be a characteristic feature within insular taxa.     

Gene flow and selection interact to promote adaptive divergence in regions of low recombination

Adaptation to new environments often occurs in the face of gene flow. Under these conditions, gene flow and recombination can impede adaptation by breaking down linkage disequilibrium between locally adapted alleles. Theory predicts that this decay can be halted or slowed if adaptive alleles are tightly linked in regions of low recombination, potentially favouring divergence and adaptive evolution in these regions over others. Here, we compiled a global genomic data set of over 1,300 individual threespine stickleback from 52 populations and compared the tendency for adaptive alleles to occur in regions of low recombination between populations that diverged with or without gene flow. In support of theory, we found that putatively adaptive alleles (F_ST and d_XY outliers) tend to occur more often in regions of low recombination in populations where divergent selection and gene flow have jointly occurred. This result remained significant when we employed different genomic window sizes, controlled for the effects of mutation rate and gene density, controlled for overall genetic differentiation, varied the genetic map used to estimate recombination and used a continuous (rather than discrete) measure of geographic distance as proxy for gene flow/shared ancestry. We argue that our study provides the first statistical evidence that the interaction of gene flow and selection biases divergence toward regions of low recombination.     

Disentangling structural genomic and behavioural barriers in a sea of connectivity

Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole‐genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord‐type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord‐type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.