The shaping of genetic variation in edge‐of‐range populations under past and future climate change

With rates of climate change exceeding the rate at which many species are able to shift their range or adapt, it is important to understand how future changes are likely to affect biodiversity at all levels of organisation. Understanding past responses and extent of niche conservatism in climatic tolerance can help predict future consequences. We use an integrated approach to determine the genetic consequences of past and future climate changes on a bat species, Plecotus austriacus. Glacial refugia predicted by palaeo‐modelling match those identified from analyses of extant genetic diversity and model‐based inference of demographic history. Former refugial populations currently contain disproportionately high genetic diversity, but niche conservatism, shifts in suitable areas and barriers to migration mean that these hotspots of genetic diversity are under threat from future climate change. Evidence of population decline despite recent northward migration highlights the need to conserve leading‐edge populations for spearheading future range shifts.     

The impact of past climate change on genetic variation and population connectivity in the Icelandic arctic fox

Previous studies have suggested that the presence of sea ice is an important factor in facilitating migration and determining the degree of genetic isolation among contemporary arctic fox populations. Because the extent of sea ice is dependent upon global temperatures, periods of significant cooling would have had a major impact on fox population connectivity and genetic variation. We tested this hypothesis by extracting and sequencing mitochondrial control region sequences from 17 arctic foxes excavated from two late-ninth-century to twelfth-century AD archaeological sites in northeast Iceland, both of which predate the Little Ice Age (approx. sixteenth to nineteenth century). Despite the fact that five haplotypes have been observed in modern Icelandic foxes, a single haplotype was shared among all of the ancient individuals. Results from simulations within an approximate Bayesian computation framework suggest that the rapid increase in Icelandic arctic fox haplotype diversity can only be explained by sea-ice-mediated fox immigration facilitated by the Little Ice Age.     

Testing the role of ancient and contemporary landscapes on structuring genetic variation in a specialist grasshopper

Understanding the processes underlying spatial patterns of genetic diversity and structure of natural populations is a central topic in evolutionary biogeography. In this study, we combine data on ancient and contemporary landscape composition to get a comprehensive view of the factors shaping genetic variation across the populations of the scrub‐legume grasshopper (Chorthippus binotatus binotatus) from the biogeographically complex region of southeast Iberia. First, we examined geographical patterns of genetic structure and employed an approximate Bayesian computation (ABC) approach to compare different plausible scenarios of population divergence. Second, we used a landscape genetic framework to test for the effects of (1) Late Miocene paleogeography, (2) Pleistocene climate fluctuations, and (3) contemporary topographic complexity on the spatial patterns of population genetic differentiation. Genetic structure and ABC analyses supported the presence of three genetic clusters and a sequential west‐to‐east splitting model that predated the last glacial maximum (LGM, c. 21 Kya). Landscape genetic analyses revealed that population genetic differentiation was primarily shaped by contemporary topographic complexity, but was not explained by any paleogeographic scenario or resistance distances based on climate suitability in the present or during the LGM. Overall, this study emphasizes the need of integrating information on ancient and contemporary landscape composition to get a comprehensive view of their relative importance to explain spatial patterns of genetic variation in organisms inhabiting regions with complex biogeographical histories.     

Markers in time and space: A review of the last decade of plant phylogeographic approaches

Plant studies comprise a relatively small proportion of the phylogeographic literature, likely as a consequence of the fundamental challenges posed by the complex genomic structures and life history strategies of these organisms. Comparative plastomics (i.e., comparisons of mutation rates within and among regions of the chloroplast genome) across plant lineages has led to an increased understanding of which markers are likely to provide the most information at low taxonomic levels. However, the extent to which the results of such work have influenced the literature has not been fully assessed, nor has the extent to which plant phylogeographers explicitly analyse markers in time and space, both of which are integral components of the field. Here, we reviewed more than 400 publications from the last decade of plant phylogeography to specifically address the following questions: (i) What is the phylogenetic breadth of studies to date? (ii) What molecular markers have been used, and why were they chosen? (iii) What kinds of markers are most frequently used and in what combinations? (iv) How frequently are divergence time estimation and ecological niche modelling used in plant phylogeography? Our results indicate that chloroplast DNA sequence data remain the primary tool of choice, followed distantly by nuclear DNA sequences and microsatellites. Less than half (42%) of all studies use divergence time estimation, while even fewer use ecological niche modelling (14%). We discuss the implications of our findings, as well as the need for community standards on data reporting.     

Postglacial recolonization history of the European crabapple (Malus sylvestris Mill.), a wild contributor to the domesticated apple

Understanding the way in which the climatic oscillations of the Quaternary Period have shaped the distribution and genetic structure of extant tree species provides insight into the processes driving species diversification, distribution and survival. Deciphering the genetic consequences of past climatic change is also critical for the conservation and sustainable management of forest and tree genetic resources, a timely endeavour as the Earth heads into a period of fast climate change. We used a combination of genetic data and ecological niche models to investigate the historical patterns of biogeographic range expansion of a wild fruit tree, the European crabapple (Malus sylvestris), a wild contributor to the domesticated apple. Both climatic predictions for the last glacial maximum and analyses of microsatellite variation indicated that M. sylvestris experienced range contraction and fragmentation. Bayesian clustering analyses revealed a clear pattern of genetic structure, with one genetic cluster spanning a large area in Western Europe and two other genetic clusters with a more limited distribution range in Eastern Europe, one around the Carpathian Mountains and the other restricted to the Balkan Peninsula. Approximate Bayesian computation appeared to be a powerful technique for inferring the history of these clusters, supporting a scenario of simultaneous differentiation of three separate glacial refugia. Admixture between these three populations was found in their suture zones. A weak isolation by distance pattern was detected within each population, indicating a high extent of historical gene flow for the European crabapple.     

Northern glacial refugia and altitudinal niche divergence shape genome‐wide differentiation in the emerging plant model Arabidopsis arenosa

Quaternary climatic oscillations profoundly impacted temperate biodiversity. For many diverse yet undersampled areas, however, the consequences of this impact are still poorly known. In Europe, particular uncertainty surrounds the role of Balkans, a major hotspot of European diversity, in postglacial recolonization of more northerly areas, and the Carpathians, a debatable candidate for a northern ‘cryptic’ glacial refugium. Using genome‐wide SNPs and microsatellites, we examined how the interplay of historical processes and niche shifts structured genetic diversity of diploid Arabidopsis arenosa, a little‐known member of the plant model genus that occupies a wide niche range from sea level to alpine peaks across eastern temperate Europe. While the northern Balkans hosted one isolated endemic lineage, most of the genetic diversity was concentrated further north in the Pannonian Basin and the Carpathians, where it likely survived the last glaciation in northern refugia. Finally, a distinct postglacial environment in northern Europe was colonized by populations of admixed origin from the two Carpathian lineages. Niche differentiation along altitude‐related bioclimatic gradients was the main trend in the phylogeny of A. arenosa. The most prominent niche shifts, however, characterized genetically only slightly divergent populations that expanded into narrowly defined alpine and northern coastal postglacial environments. Our study highlights the role of eastern central European mountains not only as refugia for unique temperate diversity but also sources for postglacial expansion into novel high‐altitude and high‐latitude niches. Knowledge of distinct genetic substructure of diploid A. arenosa also opens new opportunities for follow‐up studies of this emerging model of evolutionary biology.     

Spatiotemporally explicit demographic modelling supports a joint effect of historical barriers to dispersal and contemporary landscape composition on structuring genomic variation in a red‐listed grasshopper

Inferring the processes underlying spatial patterns of genomic variation is fundamental to understand how organisms interact with landscape heterogeneity and to identify the factors determining species distributional shifts. Here, we use genomic data (restriction site‐associated DNA sequencing) to test biologically informed models representing historical and contemporary demographic scenarios of population connectivity for the Iberian cross‐backed grasshopper Dociostaurus hispanicus, a species with a narrow distribution that currently forms highly fragmented populations. All models incorporated biological aspects of the focal taxon that could hypothetically impact its geographical patterns of genomic variation, including (a) spatial configuration of impassable barriers to dispersal defined by topographic landscapes not occupied by the species; (b) distributional shifts resulting from the interaction between the species bioclimatic envelope and Pleistocene glacial cycles; and (c) contemporary distribution of suitable habitats after extensive land clearing for agriculture. Spatiotemporally explicit simulations under different scenarios considering these aspects and statistical evaluation of competing models within an Approximate Bayesian Computation framework supported spatial configuration of topographic barriers to dispersal and human‐driven habitat fragmentation as the main factors explaining the geographical distribution of genomic variation in the species, with no apparent impact of hypothetical distributional shifts linked to Pleistocene climatic oscillations. Collectively, this study supports that both historical (i.e., topographic barriers) and contemporary (i.e., anthropogenic habitat fragmentation) aspects of landscape composition have shaped major axes of genomic variation in the studied species and emphasizes the potential of model‐based approaches to gain insights into the temporal scale at which different processes impact the demography of natural populations.     

Spatial and temporal patterns of genetic variation in the widespread antitropical deep‐sea coral Paragorgia arborea

Numerous deep‐sea species have apparent widespread and discontinuous distributions. Many of these are important foundation species, structuring hard‐bottom benthic ecosystems. Theoretically, differences in the genetic composition of their populations vary geographically and with depth. Previous studies have examined the genetic diversity of some of these taxa in a regional context, suggesting that genetic differentiation does not occur at scales of discrete features such as seamounts or canyons, but at larger scales (e.g. ocean basins). However, to date, few studies have evaluated such diversity throughout the known distribution of a putative deep‐sea species. We utilized sequences from seven mitochondrial gene regions and nuclear genetic variants of the deep‐sea coral Paragorgia arborea in a phylogeographic context to examine the global patterns of genetic variation and their possible correlation with the spatial variables of geographic position and depth. We also examined the compatibility of this morphospecies with the genealogical‐phylospecies concept by examining specimens collected worldwide. We show that the morphospecies P. arborea can be defined as a genealogical‐phylospecies, in contrast to the hypothesis that P. arborea represents a cryptic species complex. Genetic variation is correlated with geographic location at the basin‐scale level, but not with depth. Additionally, we present a phylogeographic hypothesis in which P. arborea originates from the North Pacific, followed by colonization of the Southern Hemisphere prior to migration to the North Atlantic. This hypothesis is consistent with the latest ocean circulation model for the Miocene.     

Inferring past demographic changes from contemporary genetic data: A simulation‐based evaluation of the ABC methods implemented in diyabc

Inferring the demographic history of species and their populations is crucial to understand their contemporary distribution, abundance and adaptations. The high computational overhead of likelihood‐based inference approaches severely restricts their applicability to large data sets or complex models. In response to these restrictions, approximate Bayesian computation (ABC) methods have been developed to infer the demographic past of populations and species. Here, we present the results of an evaluation of the ABC‐based approach implemented in the popular software package diyabc using simulated data sets (mitochondrial DNA sequences, microsatellite genotypes and single nucleotide polymorphisms). We simulated population genetic data under five different simple, single‐population models to assess the model recovery rates as well as the bias and error of the parameter estimates. The ability of diyabc to recover the correct model was relatively low (0.49): 0.6 for the simplest models and 0.3 for the more complex models. The recovery rate improved significantly when reducing the number of candidate models from five to three (from 0.57 to 0.71). Among the parameters of interest, the effective population size was estimated at a higher accuracy compared to the timing of events. Increased amounts of genetic data did not significantly improve the accuracy of the parameter estimates. Some gains in accuracy and decreases in error were observed for scaled parameters (e.g., N_eμ) compared to unscaled parameters (e.g., N_e and μ). We concluded that diyabc ‐based assessments are not suited to capture a detailed demographic history, but might be efficient at capturing simple, major demographic changes.     

A range-wide genetic bottleneck overwhelms contemporary landscape factors and local abundance in shaping genetic patterns of an alpine butterfly (Lepidoptera: Pieridae: Colias behrii)

Spatial and environmental heterogeneity are major factors in structuring species distributions in alpine landscapes. These landscapes have also been affected by glacial advances and retreats, causing alpine taxa to undergo range shifts and demographic changes. These nonequilibrium population dynamics have the potential to obscure the effects of environmental factors on the distribution of genetic variation. Here, we investigate how demographic change and environmental factors influence genetic variation in the alpine butterfly Colias behrii. Data from 14 microsatellite loci provide evidence of bottlenecks in all population samples. We test several alternative models of demography using approximate Bayesian computation (ABC), with the results favouring a model in which a recent bottleneck precedes rapid population growth. Applying independent calibrations to microsatellite loci and a nuclear gene, we estimate that this bottleneck affected both northern and southern populations 531–281 years ago, coinciding with a period of global cooling. Using regression approaches, we attempt to separate the effects of population structure, geographical distance and landscape on patterns of population genetic differentiation. Only 40% of the variation in F_ST is explained by these models, with geographical distance and least‐cost distance among meadow patches selected as the best predictors. Various measures of genetic diversity within populations are also decoupled from estimates of local abundance and habitat patch characteristics. Our results demonstrate that demographic change can have a disproportionate influence on genetic diversity in alpine species, contrasting with other studies that suggest landscape features control contemporary demographic processes in high‐elevation environments.     

The presence of a cryptic barrier in the West Pacific Ocean suggests the effect of glacial climate changes on a widespread sea‐dispersed plant,Vigna marina (Fabaceae)

Ocean currents are an important driver of evolution for sea‐dispersed plants, enabling them to maintain reciprocal gene flow via sea‐dispersed diaspores and obtain wide distribution ranges. Although geographic barriers are known to be the primary factors shaping present genetic structure of sea‐dispersed plants, cryptic barriers which form clear genetic structure within oceanic regions are poorly understood. To test the presence of a cryptic barrier, we conducted a phylogeographic study together with past demographic inference for a widespread sea‐dispersed plant, Vigna marina, using 308 individuals collected from the entire Indo‐West Pacific (IWP) region. Chloroplast DNA variation showed strong genetic structure that separated populations into three groups: North Pacific (NP), South Pacific (SP) and Indian Ocean (IN) (F′_CT among groups = 0.954–1.000). According to the Approximate Bayesian computation inference, splitting time between NP and SP was approximately 20,200 years (95%HPD, 4,530–95,400) before present. Moreover, a signal of recent population expansion was detected in the NP group. This study clearly showed the presence of a cryptic barrier in the West Pacific region of the distributional range of V. marina. The locations of the cryptic barrier observed in V. marina corresponded to the genetic breaks found in other plants, suggesting the presence of a common cryptic barrier for sea‐dispersed plants. Demographic inference suggested that genetic structure related to this cryptic barrier has been present since the last glacial maximum and may reflect patterns of past population expansion from refugia.     

Congruent phylogeographic patterns in a young radiation of live‐bearing marine snakes: Pleistocene vicariance and the conservation implications of cryptic genetic diversity

Aim

To investigate phylogeographic patterns among and within co‐occurring sea snake species from Australia's endemic viviparous Aipysurus lineage, which includes critically endangered species, and evaluate the conservation implications of geographically structured patterns of genetic divergence and diversity.

Location

Australia's tropical shallow water marine environments spanning four regions: Great Barrier Reef (GBR), Gulf of Carpentaria (GoC), Timor Sea (TS) and coastal WA (WAC).

Methods

Samples from >550 snakes representing all nine nominal Aipysurus group species were obtained from throughout their known Australian ranges. Coalescent phylogenetic analyses and Bayesian molecular dating of mitochondrial DNA, combined with Bayesian and traditional population genetic analyses of 11 microsatellite loci, were used to evaluate genetic divergence and diversity.

Results

Mitochondrial DNA revealed highly congruent phylogeographic breaks among co‐occurring species, largely supported by nuclear microsatellites. For each species, each region was characterized by a unique suite of haplotypes (phylogroups). Divergences between the TS, GoC and/or GBR were invariably shallow and dated as occurring 50,000–130,000 years ago, coinciding with the cyclic Pleistocene emergence of the Torres Strait land bridge. By contrast, sea snakes from coastal WA were consistently highly divergent from other regions and dated as diverging 178,000–526,000 years ago, which was not associated with any known vicariant events.

Main Conclusions

Previously unappreciated highly divergent sea snake lineages in coastal WA potentially represent cryptic species, highlighting this region as a high‐priority area for conservation. The cyclic emergence of the Torres Strait land bridge is consisted with observed divergences between the TS, GoC and/or GBR; however, processes involved in the earlier divergences involving the WAC remain to be determined. The observed strong population genetic structures (as surrogates for dispersal) indicate that sea snakes have limited potential to reverse population declines via replenishment from other sources over time frames relevant to conservation.

     

Beyond the landscape: Resistance modelling infers physical and behavioural gene flow barriers to a mobile carnivore across a metropolitan area

Urbanization affects key aspects of wildlife ecology. Dispersal in urban wildlife species may be impacted by geographical barriers but also by a species’ inherent behavioural variability. There are no functional connectivity analyses using continuous individual‐based sampling across an urban‐rural continuum that would allow a thorough assessment of the relative importance of physical and behavioural dispersal barriers. We used 16 microsatellite loci to genotype 374 red foxes (Vulpes vulpes) from the city of Berlin and surrounding rural regions in Brandenburg in order to study genetic structure and dispersal behaviour of a mobile carnivore across the urban‐rural landscape. We assessed functional connectivity by applying an individual‐based landscape genetic optimization procedure. Three commonly used genetic distance measures yielded different model selection results, with only the results of an eigenvector‐based multivariate analysis reasonably explaining genetic differentiation patterns. Genetic clustering methods and landscape resistance modelling supported the presence of an urban population with reduced dispersal across the city border. Artificial structures (railways, motorways) served as main dispersal corridors within the cityscape, yet urban foxes avoided densely built‐up areas. We show that despite their ubiquitous presence in urban areas, their mobility and behavioural plasticity, foxes were affected in their dispersal by anthropogenic presence. Distinguishing between man‐made structures and sites of human activity, rather than between natural and artificial structures, is thus essential for better understanding urban fox dispersal. This differentiation may also help to understand dispersal of other urban wildlife and to predict how behaviour can shape population genetic structure beyond physical barriers.     

Spatiotemporal analyses suggest the role of glacial history and the ice‐free corridor in shaping American badger population genetic variation

Recurring glacial cycles through the Quaternary period drastically altered the size and distribution of natural populations of North American flora and fauna. The “southerly refugia model” has been the longstanding framework for testing the effects of glaciation on contemporary genetic patterns; however, insights from ancient DNA have contributed to the reconstruction of more complex histories for some species. The American badger, Taxidea taxus, provides an interesting species for exploring the genetic legacy of glacial history, having been hypothesized to have postglacially emerged from a single, southerly refugium to recolonize northern latitudes. However, previous studies have lacked genetic sampling from areas where distinct glacial refugia have been hypothesized, including the Pacific Northwest and American Far North (Yukon, Alaska). In order to further investigate the phylogeographic history of American badgers, we collected mitochondrial DNA sequence data from ancient subfossil material collected within the historical range (Alaska, Yukon) and combined them with new and previously published data from across the species' contemporary distribution (n = 1,207). We reconstructed a mostly unresolved phylogenetic tree and star‐like haplotype network indicative of emergence from a largely panmictic glacial refugium and recent population expansion, the latter further punctuated by significantly negative Tajima's D and Fu's Fs values. Although directionality of migration cannot be unequivocally inferred, the moderate to high levels of genetic variation exhibited by American badgers, alongside the low frequency of haplotypes with indels in the Midwest, suggest a potential recolonization into central North America after the hypothesized ice‐free corridor reopened ~13,000 years ago. Overall, the expanded reconstruction of phylogeographic history of American badgers offers a broader understanding of contemporary range‐wide patterns and identifies unique genetic units that can likely be used to inform conservation of at‐risk populations at the northern periphery.     

Historical abiotic events or human‐aided dispersal: inferring the evolutionary history of a newly discovered galaxiid fish

Range expansion of obligate freshwater fishes in the Cape Floristic Region (CFR) of South Africa has mostly been attributed to river capture events and confluence of rivers following sea‐level regression. The role of low drainage divides and interbasin water transfers has received less attention. This study analyzed mitochondrial and nuclear DNA sequences to assess the processes that could have influenced the phylogeographic patterns of a newly discovered lineage of Galaxias zebratus (hereafter Galaxias zebratus “Joubertina”) that occurs across two currently isolated river systems close to the Joubertina area in the eastern CFR. Results from both analyses revealed that observed genetic differentiation cannot be explained by isolation between the two river systems. No genetic differentiation was found between the Krom River system and a population from one of the Gamtoos tributaries. Shallow genetic differentiation was found between the Krom and the other Gamtoos populations. Historical river capture events and sea‐level changes do not explain the present distribution of Galaxias zebratus “Joubertina” across the Krom and Gamtoos River systems. Interbasin dispersal during pluvial periods, recent river capture, or recent human‐mediated translocation seems to be the most plausible explanations.