Divergence in coloration and ecological speciation in the Anolis marmoratus species complex

Adaptive divergence in coloration is expected to produce reproductive isolation in species that use colourful signals in mate choice and species recognition. Indeed, many adaptive radiations are characterized by differentiation in colourful signals, suggesting that divergent selection acting on coloration may be an important component of speciation. Populations in the Anolis marmoratus species complex from the Caribbean island of Guadeloupe display striking divergence in the colour and pattern of adult males that occurs over small geographic distances, suggesting strong divergent selection. Here we test the hypothesis that divergence in coloration results in reduced gene flow among populations. We quantify variation in adult male coloration across a habitat gradient between mesic and xeric habitats, use a multilocus coalescent approach to infer historical demographic parameters of divergence, and examine gene flow and population structure using microsatellite variation. We find that colour variation evolved without geographic isolation and in the face of gene flow, consistent with strong divergent selection and that both ecological and sexual selection are implicated. However, we find no significant differentiation at microsatellite loci across populations, suggesting little reproductive isolation and high levels of contemporary gene exchange. Strong divergent selection on loci affecting coloration probably maintains clinal phenotypic variation despite high gene flow at neutral loci, supporting the notion of a porous genome in which adaptive portions of the genome remain fixed whereas neutral portions are homogenized by gene flow and recombination. We discuss the impact of these findings for studies of colour evolution and ecological speciation.     

Extinction,reintroduction, and restoration of a lizard meta‐population equilibrium in the missouri ozarks

In this issue of Molecular Ecology, Neuwald & Templeton (2013) report on a 22‐year study of natural populations of Collared Lizards (Crotaphytus collaris) that evolved on isolated on rock outcrops (‘glades’) in the Ozark Mountains in eastern Missouri. This ecosystem was originally maintained by frequent fires that kept the forest understory open, but fire‐suppression was adopted as official policy in about 1945, which led to a loss of native biodiversity, including local extinctions of some lizard populations. Policies aimed at restoring biodiversity included controlled burns and re‐introductions of lizards to some glades, which began in 1984. Populations were monitored from 1984–2006, and demographic and genetic data collected from 1 679 lizards were used to documents shifts in meta‐population dynamics over four distinct phases of lizard recovery: 1–an initial translocation of lizards drawn from the same source populations onto three glades that were likely part of one meta‐population; 2–a period of isolation and genetic drift associated with the absence of fires; 3–a period of rapid colonization and population increase following restoration of fire; and 4–stabilization of the meta‐population under regular prescribed burning. This study system thus provides a rare opportunity to characterize the dynamics of a landscape‐scale management strategy on the restoration of the meta‐population of a reintroduced species; long‐term case studies of the extinction, founding, increase, and stabilization of a well‐defined meta‐population, based on both demographic and population genetic data, are rare in the conservation, ecological, and evolutionary literature.     

netview p: a network visualization tool to unravel complex population structure using genome‐wide SNPs

Network‐based approaches are emerging as valuable tools for the analysis of complex genetic structure in wild and captive populations. netview p combines data quality control with the construction of population networks through mutual k‐nearest neighbours thresholds applied to genome‐wide SNPs. The program is cross‐platform compatible, open‐source and efficiently operates on data ranging from hundreds to hundreds of thousands of SNPs. The pipeline was used for the analysis of pedigree data from simulated (n = 750, SNPs = 1279) and captive silver‐lipped pearl oysters (n = 415, SNPs = 1107), wild populations of the European hake from the Atlantic and Mediterranean (n = 834, SNPs = 380) and grey wolves from North America (n = 239, SNPs = 78 255). The population networks effectively visualize large‐ and fine‐scale genetic structure within and between populations, including family‐level structure and relationships. netview p comprises a network‐based addition to other population analysis tools and provides user‐friendly access to a complex network analysis pipeline through implementation in python .     

Habitat continuity and stepping‐stone oceanographic distances explain population genetic connectivity of the brown alga Cystoseira amentacea

Effective predictive and management approaches for species occurring in a metapopulation structure require good understanding of interpopulation connectivity. In this study, we ask whether population genetic structure of marine species with fragmented distributions can be predicted by stepping‐stone oceanographic transport and habitat continuity, using as model an ecosystem‐structuring brown alga, Cystoseira amentacea var. stricta. To answer this question, we analysed the genetic structure and estimated the connectivity of populations along discontinuous rocky habitat patches in southern Italy, using microsatellite markers at multiple scales. In addition, we modelled the effect of rocky habitat continuity and ocean circulation on gene flow by simulating Lagrangian particle dispersal based on ocean surface currents allowing multigenerational stepping‐stone dynamics. Populations were highly differentiated, at scales from few metres up to thousands of kilometres. The best possible model fit to explain the genetic results combined current direction, rocky habitat extension and distance along the coast among rocky sites. We conclude that a combination of variable suitable habitat and oceanographic transport is a useful predictor of genetic structure. This relationship provides insight into the mechanisms of dispersal and the role of life‐history traits. Our results highlight the importance of spatially explicit modelling of stepping‐stone dynamics and oceanographic directional transport coupled with habitat suitability, to better describe and predict marine population structure and differentiation. This study also suggests the appropriate spatial scales for the conservation, restoration and management of species that are increasingly affected by habitat modifications.     

Canadian polar bear population structure using genome‐wide markers

Predicting the consequences of environmental changes, including human‐mediated climate change on species, requires that we quantify range‐wide patterns of genetic diversity and identify the ecological, environmental, and historical factors that have contributed to it. Here, we generate baseline data on polar bear population structure across most Canadian subpopulations (n = 358) using 13,488 genome‐wide single nucleotide polymorphisms (SNPs) identified with double‐digest restriction site‐associated DNA sequencing (ddRAD). Our ddRAD dataset showed three genetic clusters in the sampled Canadian range, congruent with previous studies based on microsatellites across the same regions; however, due to a lack of sampling in Norwegian Bay, we were unable to confirm the existence of a unique cluster in that subpopulation. These data on the genetic structure of polar bears using SNPs provide a detailed baseline against which future shifts in population structure can be assessed, and opportunities to develop new noninvasive tools for monitoring polar bears across their range.     

High‐throughput SNPs for all: genotyping‐in‐thousands

Understanding the genetic structure of species is essential for conservation. It is only with this information that managers, academics, user groups and land‐use planners can understand the spatial scale of migration and local adaptation, source‐sink dynamics and effective population size. Such information is essential for a multitude of applications including delineating management units, balancing management priorities, discovering cryptic species and implementing captive breeding programmes. Species can range from locally adapted by hundreds of metres (Pavey et al. 2010 ) to complete species panmixia (Côté et al. 2013 ). Even more remarkable is that this essential information can be obtained without fully sequenced or annotated genomes, but from mere (putatively) nonfunctional variants. First with allozymes, then microsatellites and now SNPs, this neutral genetic variation carries a wealth of information about migration and drift. For many of us, it may be somewhat difficult to remember our understanding of species conservation before the widespread usage of these useful tools. However most species on earth have yet to give us that ‘peek under the curtain’. With the current diversity on earth estimated to be nearly 9 million species (Mora et al. 2011 ), we have a long way to go for a comprehensive meta‐phylogeographic understanding. A method presented in this issue by Campbell and colleagues (Campbell et al. 2015 ) is a tool that will accelerate the pace in this area. Genotyping‐in‐thousands (GT‐seq) leverages recent advancements in sequencing technology to save many hours and dollars over previous methods to generate this important neutral genetic information.     

Speciation,population structure,and demographic history of the Mojave Fringe‐toed Lizard (Uma scoparia), a species of conservation concern

The North American deserts were impacted by both Neogene plate tectonics and Quaternary climatic fluctuations, yet it remains unclear how these events influenced speciation in this region. We tested published hypotheses regarding the timing and mode of speciation, population structure, and demographic history of the Mojave Fringe‐toed Lizard (Uma scoparia), a sand dune specialist endemic to the Mojave Desert of California and Arizona. We sampled 109 individual lizards representing 22 insular dune localities, obtained DNA sequences for 14 nuclear loci, and found that U. scoparia has low genetic diversity relative to the U. notata species complex, comparable to that of chimpanzees and southern elephant seals. Analyses of genotypes using Bayesian clustering algorithms did not identify discrete populations within U. scoparia. Using isolation‐with‐migration (IM) models and a novel coalescent‐based hypothesis testing approach, we estimated that U. scoparia diverged from U. notata in the Pleistocene epoch. The likelihood ratio test and the Akaike Information Criterion consistently rejected nested speciation models that included parameters for migration and population growth of U. scoparia. We reject the Neogene vicariance hypothesis for the speciation of U. scoparia and define this species as a single evolutionarily significant unit for conservation purposes.     

Bridging the gap: western rock skinks (Trachylepis sulcata) have a short history in South Africa

Phylogeographic patterns in wide-ranging species in southern Africa remain largely unexplored, especially in areas north of South Africa. Here, we investigate population structuring, demographic history, and the colonization pattern of the western rock skink (Trachylepis sulcata), a rock-dwelling species with a range extending from southwestern South Africa into Angola. Using 1056 bp from the mitochondrial marker ND2 and > 2.5 kb from three nuclear genes (EXPH5, KIF24, RAG-1), we constructed allele networks, generated extended Bayesian skyline plots and performed population clustering analyses. Analyses of historical demographic patterns show an overall southward range expansion from Northern Namibia into Southern Namibia and South Africa, although we find contrasting genetic breaks across these geographic regions using nuclear and mitochondrial data. We suggest that mtDNA has introgressed across a nuclear break corresponding to the Knersvlakte region of South Africa, a previously proposed biogeographic barrier for rupicolous species. This pattern of mitochondrial variation contrasts sharply to that of other South African taxa previously investigated, which all show significant mtDNA differentiation across the Knersvlakte region. Additionally, while other taxa show divergences dating to the Pliocene, T. sulcata appears to be a recent arrival in southern Africa, having crossed this barrier and colonized South Africa in the mid-Pleistocene. The complex phylogeographic history of T. sulcata corroborates the intricate patterns of genetic variation found in South African taxa and provides novel insight into historical processes affecting species distributed across Namibia.     

Divergence with gene flow in a population of thermophilic bacteria: a potential role for spatially varying selection

A fundamental goal of evolutionary biology is to understand how ecological diversity arises and is maintained in natural populations. We have investigated the contributions of gene flow and divergent selection to the distribution of genetic variation in an ecologically differentiated population of a thermophilic cyanobacterium (Mastigocladus laminosus) found along the temperature gradient of a nitrogen‐limited stream in Yellowstone National Park. For most loci sampled, gene flow appears to be sufficient to prevent substantial genetic divergence. However, one locus (rfbC) exhibited a comparatively low migration rate as well as other signatures expected for a gene experiencing spatially varying selection, including an excess of common variants, an elevated level of polymorphism and extreme genetic differentiation along the gradient. rfbC is part of an expression island involved in the production of the polysaccharide component of the protective envelope of the heterocyst, the specialized nitrogen‐fixing cell of these bacteria. SNP genotyping in the vicinity of rfbC revealed a ~5‐kbp region including a gene content polymorphism that is tightly associated with environmental temperature and therefore likely contains the target of selection. Two genes have been deleted both in the predominant haplotype found in the downstream region of White Creek and in strains from other Yellowstone populations of M. laminosus, which may result in the production of heterocysts with different envelope properties. This study implicates spatially varying selection in the maintenance of variation related to thermal performance at White Creek despite on‐going or recent gene flow.     

Conservation genetics and population history of the threatened European mink Mustela lutreola, with an emphasis on the west European population

In species of great conservation concern, special attention must be paid to their phylogeography, in particular the origin of animals for captive breeding and reintroduction. The endangered European mink lives now in at least three well-separated populations in northeast, southeast and west Europe. Our aim is to assess the genetic structure of these populations to identify 'distinct population segments' (DPS) and advise captive breeding programmes. First, the mtDNA control region was completely sequenced in 176 minks and 10 polecats. The analysis revealed that the western population is characterized by a single mtDNA haplotype that is closely related to those in eastern regions but nevertheless, not found there to date. The northeast European animals are much more variable (pi = 0.012, h = 0.939), with the southeast samples intermediate (pi = 0.0012, h = 0.469). Second, 155 European mink were genotyped using six microsatellites. The latter display the same trends of genetic diversity among regions as mtDNA [gene diversity and allelic richness highest in northeast Europe (H(E) = 0.539, R(S) = 3.76), lowest in west Europe (H(E) = 0.379, R(S) = 2.12)], and provide evidences that the southeast and possibly the west populations have undergone a recent bottleneck. Our results indicate that the western population derives from a few animals which recently colonized this region, possibly after a human introduction. Microsatellite data also reveal that isolation by distance occurs in the western population, causing some inbreeding because related individuals mate. As genetic data indicate that the three populations have not undergone independent evolutionary histories for long (no phylogeographical structure), they should not be considered as distinct DPS. In conclusion, the captive breeding programme should use animals from different parts of the species' present distribution area.     

metapop2: Re‐implementation of software for the analysis and management of subdivided populations using gene and allelic diversity

Management programmes often have to make decisions based on the analysis of the genetic properties and diversity of populations. Expected heterozygosity (or gene diversity) and population structure parameters are often used to make recommendations for conservation, such as avoidance of inbreeding or migration across subpopulations. Allelic diversity, however, can also provide complementary and useful information for conservation programmes, as it is highly sensitive to population bottlenecks, and is more related to long‐term selection response than heterozygosity. Here we present a completely revised and updated re‐implementation of the software metapop for the analysis of diversity in subdivided populations, as well as a tool for the management and dynamic estimation of optimal contributions in conservation programmes. This new update includes computation of allelic diversity for population analysis and management, as well as a simulation mode to forecast the consequences of taking different management strategies over time. Furthermore, the new implementation in C++ includes code optimization and improved memory usage, allowing for fast analysis of large data sets including single nucleotide polymorphism markers, as well as enhanced cross‐software and cross‐platform compatibility.     

Estimating population structure under nonequilibrium conditions in a conservation context: continent-wide population genetics of the giant Amazon river turtle, Podocnemis expansa (Chelonia; Podocnemididae)

Giant Amazon river turtles, Podocnemis expansa, are indigenous to the Amazon, Orinoco, and Essequibo River basins, and are distributed across nearly the entire width of the South American continent. Although once common, their large size, high fecundity, and gregarious nesting, made P. expansa especially vulnerable to over-harvesting for eggs and meat. Populations have been severely reduced or extirpated in many areas throughout its range, and the species is now regulated under Appendix II of the Convention on International Trade in Endangered Species. Here, we analyse data from mitochondrial DNA sequence and multiple nuclear microsatellite markers with an array of complementary analytical methods. Results show that concordance from multiple data sets and analyses can provide a strong signal of population genetic structure that can be used to guide management. The general lack of phylogeographic structure but large differences in allele and haplotype frequencies among river basins is consistent with fragmented populations and female natal-river homing. Overall, the DNA data show that P. expansa populations lack a long history of genetic differentiation, but that each major tributary currently forms a semi-isolated reproductive population and should be managed accordingly.     

Genetic diversity and recombination in natural populations of the nematode‐trapping fungus Arthrobotrys oligospora from China

Nematophagous fungi can trap and capture nematodes and other small invertebrates. This unique ability has made them ideal organisms from which to develop biological control agents against plant‐ and animal‐parasitic nematodes. However, effective application of biocontrol agents in the field requires a comprehensive understanding about the ecology and population genetics of the nematophagous fungi in natural environments. Here, we genotyped 228 strains of the nematode‐trapping fungus Arthrobotrys oligospora using 12 single nucleotide polymorphic markers located on eight random DNA fragments. The strains were from different ecological niches and geographical regions from China. Our analyses identified that ecological niche separations contributed significantly, whereas geographic separation contributed relatively little to the overall genetic variation in our samples of A. oligospora. Interestingly, populations from stressful environments seemed to be more variable and showed more evidence for recombination than those from benign environments at the same geographic areas. We discussed the implications of our results to the conservation and biocontrol application of A. oligospora in agriculture and forestry.     

A test of the central–marginal hypothesis using population genetics and ecological niche modelling in an endemic salamander (Ambystoma barbouri)

The central–marginal hypothesis (CMH) predicts that population size, genetic diversity and genetic connectivity are highest at the core and decrease near the edges of species' geographic distributions. We provide a test of the CMH using three replicated core‐to‐edge transects that encompass nearly the entire geographic range of the endemic streamside salamander (Ambystoma barbouri). We confirmed that the mapped core of the distribution was the most suitable habitat using ecological niche modelling (ENM) and via genetic estimates of effective population sizes. As predicted by the CMH, we found statistical support for decreased genetic diversity, effective population size and genetic connectivity from core to edge in western and northern transects, yet not along a southern transect. Based on our niche model, habitat suitability is lower towards the southern range edge, presumably leading to conflicting core‐to‐edge genetic patterns. These results suggest that multiple processes may influence a species' distribution based on the heterogeneity of habitat across a species' range and that replicated sampling may be needed to accurately test the CMH. Our work also emphasizes the importance of identifying the geographic range core with methods other than using the Euclidean centre on a map, which may help to explain discrepancies among other empirical tests of the CMH. Assessing core‐to‐edge population genetic patterns across an entire species' range accompanied with ENM can inform our general understanding of the mechanisms leading to species' geographic range limits.     

Life‐history predicts past and present population connectivity in two sympatric sea stars

Life‐history traits, especially the mode and duration of larval development, are expected to strongly influence the population connectivity and phylogeography of marine species. Comparative analysis of sympatric, closely related species with differing life histories provides the opportunity to specifically investigate these mechanisms of evolution but have been equivocal in this regard. Here, we sample two sympatric sea stars across the same geographic range in temperate waters of Australia. Using a combination of mitochondrial DNA sequences, nuclear DNA sequences, and microsatellite genotypes, we show that the benthic‐developing sea star, Parvulastra exigua, has lower levels of within‐ and among‐population genetic diversity, more inferred genetic clusters, and higher levels of hierarchical and pairwise population structure than Meridiastra calcar, a species with planktonic development. While both species have populations that have diverged since the middle of the second glacial period of the Pleistocene, most P. exigua populations have origins after the last glacial maxima (LGM), whereas most M. calcar populations diverged long before the LGM. Our results indicate that phylogenetic patterns of these two species are consistent with predicted dispersal abilities; the benthic‐developing P. exigua shows a pattern of extirpation during the LGM with subsequent recolonization, whereas the planktonic‐developing M. calcar shows a pattern of persistence and isolation during the LGM with subsequent post‐Pleistocene introgression.     

Identifying the number of population clusters with structure: problems and solutions

The program structure has been used extensively to understand and visualize population genetic structure. It is one of the most commonly used clustering algorithms, cited over 11 500 times in Web of Science since its introduction in 2000. The method estimates ancestry proportions to assign individuals to clusters, and post hoc analyses of results may indicate the most likely number of clusters, or populations, on the landscape. However, as has been shown in this issue of Molecular Ecology Resources by Puechmaille ( 2016 ), when sampling is uneven across populations or across hierarchical levels of population structure, these post hoc analyses can be inaccurate and identify an incorrect number of population clusters. To solve this problem, Puechmaille ( 2016 ) presents strategies for subsampling and new analysis methods that are robust to uneven sampling to improve inferences of the number of population clusters.     

Repetitive sequences in phylogeographic inference: a reply to Saltonstall and Lambertini (2012)

In 2011, Vachon and Freeland presented the results of a study that illustrated the importance of considering mutation patterns, including the potential for homoplasy, when deciding whether to include or exclude repetitive sequences from phylogeographic inferences. Saltonstall and Lambertini (2012) criticized this study by suggesting that some of the analyses and interpretations were flawed. In this reply, we explain why we disagree with most of their criticisms and identify some inconsistencies in their analyses. Most importantly, we reiterate the need to examine underlying assumptions, particularly with respect to mutation patterns, when using molecular genetic data to untangle evolutionary relationships.     

Adaptive divergence along environmental gradients in a climate‐change‐sensitive mammal

In the face of predicted climate change, a broader understanding of biotic responses to varying environments has become increasingly important within the context of biodiversity conservation. Local adaptation is one potential option, yet remarkably few studies have harnessed genomic tools to evaluate the efficacy of this response within natural populations. Here, we show evidence of selection driving divergence of a climate‐change‐sensitive mammal, the American pika (Ochotona princeps), distributed along elevation gradients at its northern range margin in the Coast Mountains of British Columbia (BC), Canada. We employed amplified‐fragment‐length‐polymorphism‐based genomic scans to conduct genomewide searches for candidate loci among populations inhabiting varying environments from sea level to 1500 m. Using several independent approaches to outlier locus detection, we identified 68 candidate loci putatively under selection (out of a total 1509 screened), 15 of which displayed significant associations with environmental variables including annual precipitation and maximum summer temperature. These candidate loci may represent important targets for predicting pika responses to climate change and informing novel approaches to wildlife conservation in a changing world.