Morphological and genetic differentiation in anadromous smelt Osmerus mordax (Mitchill): disentangling the effects of geography and morphology on gene flow

Morphological analyses were combined with genetic analyses at nine microsatellite loci to examine the determinants of gene flow at 21 spawning locations of rainbow smelt Osmerus mordax along the east coast of Canada. Associations between morphology, geography and gene flow were examined using a computational geometric approach and partial Mantel tests. Significant barriers to gene flow and discontinuities in morphology were observed between Newfoundland and mainland Canada, as well as within Newfoundland samples. On regional scales, contrasting patterns were present with restricted gene flow between Newfoundland populations ( F _ST= c . 0·11) and high gene flow between mainland populations ( F _ST= c . 0·017). Within Newfoundland populations, geographic distance was significantly associated with gene flow ( r = 0·85, P < 0·001) contrasting mainland samples where gene flow was most associated with phenotypic divergence ( r = 0·33, P < 0·001). At large spatial scales, weak ( r = 0·19, P = 0·02) associations between gene flow and geographic distance were observed, and moderate associations were also observed between gene flow and morphology ( r = 0·28, P < 0·001). The presence of significant genetic isolation by distance in Newfoundland samples and the clear discontinuity associated with the Cabot Strait suggest geography may be the primary determinant of gene flow. Interestingly, the association between genetic and morphological divergence within mainland samples and overall, supports the hypothesis that gene flow may be moderated by morphological divergence at larger spatial scales even in high gene flow environments.     

Population differentiation and restricted gene flow in Spanish crossbills: not isolation-by-distance but isolation-by-ecology

Divergent selection stemming from environmental variation may induce local adaptation and ecological speciation whereas gene flow might have a homogenizing effect. Gene flow among populations using different environments can be reduced by geographical distance (isolation-by-distance) or by divergent selection stemming from resource use (isolation-by-ecology). We tested for and encountered phenotypic and genetic divergence among Spanish crossbills utilizing different species of co-occurring pine trees as their food resource. Morphological, vocal and mtDNA divergence were not correlated with geographical distance, but they were correlated with differences in resource use. Resource diversity has now been found to repeatedly predict crossbill diversity. However, when resource use is not 100% differentiated, additional characters (morphological, vocal, genetic) must be used to uncover and validate hidden population structure. In general, this confirms that ecology drives adaptive divergence and limits neutral gene flow as the first steps towards ecological speciation, unprevented by a high potential for gene flow.     

Pleistocene speciation with and without gene flow in Euphaea damselflies of subtropical and tropical East Asian islands

Climatic oscillations during the Pleistocene period could have had a profound impact on the origin of tropical species by the alternation of allopatric isolation and interpopulation gene flow cycles. However, whether tropical speciation involves strictly allopatric isolation, or proceeds in the face of homogenizing gene flow, is relatively unclear. Here, we investigated geographical modes of speciation in four closely related Euphaea damselfly species endemic to the subtropical and tropical East Asian islands using coalescent analyses of a multilocus data set. The reconstructed phylogenies demonstrated distinct species status for each of the four species and the existence of two sister species pairs, Euphaea formosa/E. yayeyamana and E. decorata/E. ornata. The species divergence time of the sibling Euphaea damselflies dates back to within the last one Mya of the Middle to Lower Pleistocene. The speciation between the populous E. formosa of Taiwan and the less numerous E. yayeyamana of the Yaeyama islands occurred despite significant bidirectional, asymmetric gene flow, which is strongly inconsistent with a strictly allopatric model. In contrast, speciation of the approximately equal-sized populations of E. decorata of the southeast Asian mainland and E. ornata of Hainan is inferred to have involved allopatric divergence without gene flow. Our findings suggest that differential selection of natural or sexual environments is a prominent driver of species divergence in subtropical E. formosa and E. yayeyamana; whereas for tropical E. decorata and E. ornata at lower latitudes, allopatric isolation may well be a pivotal promoter of species formation.     

In-stream and overland dispersal across a river network influences gene flow in a freshwater insect, Calopteryx splendens

Gene flow in riverine species is constrained by the dendritic (branching) structure of the river network. Spatial genetic structure (SGS) of freshwater insects is particularly influenced by catchment characteristics and land use in the surroundings of the river. Gene flow also depends on the life cycle of organisms. Aquatic larvae mainly drift downstream whereas flying adults can disperse actively overland and along watercourses. In-stream movements can generate isolation by distance (IBD) at a local scale and differentiation between subcatchments. However, these patterns can be disrupted by overland dispersal. We studied SGS across the Loire River in the damselfly Calopteryx splendens which is able to disperse along and between watercourses. Our sampling design allowed us to test for overland dispersal effects on genetic differentiation between watercourses. Amplified fragment length polymorphism markers revealed high genetic differentiation at the catchment scale but the genetic structure did not reflect the geographical structure of sampling sites. We observed IBD patterns when considering the distance following the watercourse but also the Euclidean distance, i.e. the shortest distance, between pairs of sites. Altogether, our results support the hypothesis of overland dispersal between watercourses. From a conservation perspective, attention should be paid to the actual pathways of gene flow across complex landscapes such as river networks.     

Testing evolutionary hypotheses for phenotypic divergence using landscape genetics

Understanding the evolutionary causes of phenotypic variation among populations has long been a central theme in evolutionary biology. Several factors can influence phenotypic divergence, including geographic isolation, genetic drift, divergent natural or sexual selection, and phenotypic plasticity. But the relative importance of these factors in generating phenotypic divergence in nature is still a tantalizing and unresolved problem in evolutionary biology. The origin and maintenance of phenotypic divergence is also at the root of many ongoing debates in evolutionary biology, such as the extent to which gene flow constrains adaptive divergence ( Garant et al. 2007 ) and the relative importance of genetic drift, natural selection, and sexual selection in initiating reproductive isolation and speciation ( Coyne & Orr 2004 ). In this issue, Wang & Summers (2010) test the causes of one of the most fantastic examples of phenotypic divergence in nature: colour pattern divergence among populations of the strawberry poison frog (Dendrobates pumilio) in Panama and Costa Rica ( Fig. 1 ). This study provides a beautiful example of the use of the emerging field of landscape genetics to differentiate among hypotheses for phenotypic divergence. Using landscape genetic analyses, Wang & Summers were able to reject the hypotheses that colour pattern divergence is due to isolation‐by‐distance (IBD) or landscape resistance. Instead, the hypothesis left standing is that colour divergence is due to divergent selection, in turn driving reproductive isolation among populations with different colour morphs. More generally, this study provides a wonderful example of how the emerging field of landscape genetics, which has primarily been applied to questions in conservation and ecology, now plays an essential role in evolutionary research.

Figure 1 Open in figure viewer PowerPoint Divergent colour morphs observed among populations of the strawberry poison frog, Dendrobates pumilio. Frogs are from San Cristobal (upper left), Cerro Brujo (upper right), Bastimentos (lower right), and Agua (lower left).     

Divergent natural selection with gene flow along major environmental gradients in Amazonia: insights from genome scans, population genetics and phylogeography of the characin fish Triportheus albus

The unparalleled diversity of tropical ecosystems like the Amazon Basin has been traditionally explained using spatial models within the context of climatic and geological history. Yet, it is adaptive genetic diversity that defines how species evolve and interact within an ecosystem. Here, we combine genome scans, population genetics and sequence-based phylogeographic analyses to examine spatial and ecological arrangements of selected and neutrally evolving regions of the genome of an Amazonian fish, Triportheus albus. Using a sampling design encompassing five major Amazonian rivers, three hydrochemical settings, 352 nuclear markers and two mitochondrial DNA genes, we assess the influence of environmental gradients as biodiversity drivers in Amazonia. We identify strong divergent natural selection with gene flow and isolation by environment across craton (black and clear colour)- and Andean (white colour)-derived water types. Furthermore, we find that heightened selection and population genetic structure present at the interface of these water types appears more powerful in generating diversity than the spatial arrangement of river systems and vicariant biogeographic history. The results from our study challenge assumptions about the origin and distribution of adaptive and neutral genetic diversity in tropical ecosystems. In addition, they have important implications for measures of biodiversity and evolutionary potential in one of the world's most diverse and iconic ecosystems.     

Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies

Cave organisms occupy a special place in evolutionary biology because convergent morphologies of many species demonstrate repeatability in evolution even as they obscure phylogenetic relationships. The origin of specialized cave-dwelling species also raises the issue of the relative importance of isolation vs. natural selection in speciation. Two alternative hypotheses describe the origin of subterranean species. The 'climate-relict' model proposes allopatric speciation after populations of cold-adapted species become stranded in caves due to climate change. The 'adaptive-shift' model proposes parapatric speciation driven by divergent selection between subterranean and surface habitats. Our study of the Tennessee cave salamander complex shows that the three nominal forms (Gyrinophilus palleucus palleucus, G. p. necturoides, and G. gulolineatus) arose recently and are genealogically nested within the epigean (surface-dwelling) species, G. porphyriticus. Short branch lengths and discordant gene trees were consistent with a complex history involving gene flow between diverging forms. Results of coalescent-based analysis of the distribution of haplotypes among groups reject the allopatric speciation model and support continuous or recurrent genetic exchange during divergence. These results strongly favour the hypothesis that Tennessee cave salamanders originated from spring salamanders via divergence with gene flow.     

Perspectives and challenges in landscape genetics

A recent workshop held at the University of Grenoble gathered the leading experts in the field of landscape genetics and spatial statistics. Landscape genetics was only recently defined as an independent research field. It aims to understand the processes of gene flow and local adaptation by studying the interactions between genetic and spatial or environmental variation. This workshop discussed the perspectives and challenges of combining emerging molecular, spatial and statistical tools to unravel how landscape and environmental variables affect genetic variation.     

Speciation with gene flow and the genetics of habitat transitions

Whether speciation can advance to completion in the face of initially high levels of gene flow is a very controversial topic in evolutionary biology. Extensive gene exchange is generally considered to homogenize populations and counteract divergence. Moreover, the role of introgressive hybridization in evolution remains largely unexplored in animals, particularly in freshwater zooplankton in which allopatric speciation is considered to be the norm. Our work investigates the genetic structure of two young ecological species: the pond species, Daphnia pulex and the lake species, Daphnia pulicaria. Phylogenetic and population genetics analyses were conducted on mitochondrial NADH dehydrogenase 5 (ND5) gene, the nuclear Lactate dehydrogenase (Ldh) gene and 21 nuclear microsatellite markers in 416 individuals from habitats with various degrees of permanence. The strong and consistent phylogenetic discordance between nuclear and mitochondrial markers suggests a complex evolutionary history of multiple independent habitat transition events that involved hybridization and introgression between lake and pond Daphnia. On the other hand, the low level of contemporary gene flow between adjacent populations indicates the presence of effective habitat isolating barriers. The Daphnia system provides strong evidence for a divergence-with-gene flow speciation model that involves multiple habitat transition events.     

A parapatric propensity for breeding precludes the completion of speciation in common teal (Anas crecca, sensu lato)

Speciation is a process in which genetic drift and selection cause divergence over time. However, there is no rule dictating the time required for speciation, and even low levels of gene flow hinder divergence, so that taxa may be poised at the threshold of speciation for long periods of evolutionary time. We sequenced mitochondrial DNA (mtDNA) and eight nuclear introns (nuDNA) to estimate genomic levels of differentiation and gene flow between the Eurasian common teal (Anas crecca crecca) and the North American green‐winged teal (Anas crecca carolinensis). These ducks come into contact in Beringia (north‐eastern Asia and north‐western North America) and have probably done so, perhaps cyclically, since the Pliocene–Pleistocene transition, ～2.6 Ma, when they apparently began diverging. They have diagnosable differences in male plumage and are 6.9% divergent in the mtDNA control region, with only 1 of 58 crecca and 2 of 86 carolinensis having haplotypes grouping with the other. Two nuclear loci were likewise strongly structured between these teal (Φ_st ≥ 0.35), but six loci were undifferentiated or only weakly structured (Φ_st = 0.0–0.06). Gene flow between crecca and carolinensis was ～1 individual per generation in both directions in mtDNA, but was asymmetrical in nuDNA, with ～1 and ～20 individuals per generation immigrating into crecca and carolinensis, respectively. This study illustrates that species delimitation using a single marker oversimplifies the complexity of the speciation process, and it suggests that even with divergent selection, moderate levels of gene flow may stall the speciation process short of completion.     

Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation

Disentangling evolutionary forces that may interact to determine the patterns of genetic differentiation within and among wild populations is a major challenge in evolutionary biology. The objective of this study was to assess the genetic structure and the potential influence of several ecological variables on the extent of genetic differentiation at multiple spatial scales in a widely distributed species, the Atlantic salmon, Salmo salar . A total of 2775 anadromous fish were sampled from 51 rivers along the North American Atlantic coast and were genotyped using 13 microsatellites. A Bayesian analysis clustered these populations into seven genetically and geographically distinct groups, characterized by different environmental and ecological factors, mainly temperature. These groups were also characterized by different extent of genetic differentiation among populations. Dispersal was relatively high and of the same magnitude within compared to among regional groups, which contrasted with the maintenance of a regional genetic structure. However, genetic differentiation was lower among populations exchanging similar rates of local as opposed to inter-regional migrants, over the same geographical scale. This raised the hypothesis that gene flow could be constrained by local adaptation at the regional scale. Both coastal distance and temperature regime were found to influence the observed genetic structure according to landscape genetic analyses. The influence of other factors such as latitude, river length and altitude, migration tactic, and stocking was not significant at any spatial scale. Overall, these results suggested that the interaction between gene flow and thermal regime adaptation mainly explained the hierarchical genetic structure observed among Atlantic salmon populations.     

Ecological divergence in the presence of gene flow in two closely related Oryza species (Oryza rufipogon and O. nivara)

Ecological divergence plays a prominent role in the process of speciation, but how divergence occurs in the face of gene flow is still less clear, and remains controversial among evolutionists. Here we investigated the nucleotide diversity, divergence and gene flow between Oryza nivara and O. rufipogon using sequences of seven chloroplast and nuclear loci. By analysing samples from 26 wild populations across the geographic ranges of the two species, we showed that both species were highly structured and O. rufipogon maintained a higher level of species‐wide diversity than O. nivara. Notably, phylogenetic, amova and F_ST analyses were unable to detect significant nucleotide differentiation between the two species. We estimated that the two species began to diverge at c. 0.16 million years ago. Our coalescent‐based simulations strongly rejected the simple isolation model of zero migration between species, but rather provided unambiguous evidence of bidirectional gene flow between species, particularly from O. rufipogon to O. nivara. Our simulations also indicated that gene flow was recurrent during the divergence process rather than arising from secondary contact after allopatric divergence. In conjunction with different morphological and life‐history traits and habitat preference in the two species, this study supports the hypothesis that these Oryza species are better treated as ecotypes that diverged quite recently and are still under the process of divergence. Importantly, we demonstrate the ecological divergence between O. rufipogon and O. nivara in the presence of significant gene flow, implying that natural selection plays a primary role in driving the divergence of the two Oryza species.     

Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin's finches

Divergence and speciation can sometimes proceed in the face of, and even be enhanced by, ongoing gene flow. We here study divergence with gene flow in Darwin''s finches, focusing on the role of ecological/adaptive differences in maintaining/promoting divergence and reproductive isolation. To this end, we survey allelic variation at 10 microsatellite loci for 989 medium ground finches (Geospiza fortis) on Santa Cruz Island, Galápagos. We find only small genetic differences among G. fortis from different sites. We instead find noteworthy genetic differences associated with beak. Moreover, G. fortis at the site with the greatest divergence in beak size also showed the greatest divergence at neutral markers; i.e. the lowest gene flow. Finally, morphological and genetic differentiation between the G. fortis beak-size morphs was intermediate to that between G. fortis and its smaller (Geospiza fuliginosa) and larger (Geospiza magnirostris) congeners. We conclude that ecological differences associated with beak size (i.e. foraging) influence patterns of gene flow within G. fortis on a single island, providing additional support for ecological speciation in the face of gene flow. Patterns of genetic similarity within and between species also suggest that interspecific hybridization might contribute to the formation of beak-size morphs within G. fortis.