Testing models of speciation from genome sequences: divergence and asymmetric admixture in Island South‐East Asian Sus species during the Plio‐Pleistocene climatic fluctuations

In many temperate regions, ice ages promoted range contractions into refugia resulting in divergence (and potentially speciation), while warmer periods led to range expansions and hybridization. However, the impact these climatic oscillations had in many parts of the tropics remains elusive. Here, we investigate this issue using genome sequences of three pig (Sus) species, two of which are found on islands of the Sunda‐shelf shallow seas in Island South‐East Asia (ISEA). A previous study revealed signatures of interspecific admixture between these Sus species (Genome biology, 14 , 2013, R107). However, the timing, directionality and extent of this admixture remain unknown. Here, we use a likelihood‐based model comparison to more finely resolve this admixture history and test whether it was mediated by humans or occurred naturally. Our analyses suggest that interspecific admixture between Sunda‐shelf species was most likely asymmetric and occurred long before the arrival of humans in the region. More precisely, we show that these species diverged during the late Pliocene but around 23% of their genomes have been affected by admixture during the later Pleistocene climatic transition. In addition, we show that our method provides a significant improvement over D‐statistics which are uninformative about the direction of admixture.     

Landscape models for nuclear genetic diversity and genetic structure in white-footed mice (Peromyscus leucopus)

Dramatic changes in the North American landscape over the last 12 000 years haveshaped the genomes of the small mammals, such as the white-footed mouse (Peromyscusleucopus), which currently inhabit the region. However, very recent interactions ofpopulations with each other and the environment are expected to leave the most pronouncedsignature on rapidly evolving nuclear microsatellite loci. We analyzed landscapecharacteristics and microsatellite markers of P. leucopus populations along atransect from southern Ohio to northern Michigan, in order to evaluate hypotheses aboutthe spatial distribution of genetic heterogeneity. Genetic diversity increased to thenorth and was best approximated by a single-variable model based on habitat availabilitywithin a 0.5-km radius of trapping sites. Interpopulation differentiation measured byclustering analysis was highly variable and not significantly related to latitude orhabitat availability. Interpopulation differentiation measured as F_STvalues and chord distance was correlated with the proportion of habitat intervening, butwas best explained by agricultural distance and by latitude. The observed gradients indiversity and interpopulation differentiation were consistent with recent habitatavailability being the major constraint on effective population size in this system, andcontradicted the predictions of both the postglacial expansion and core-peripheryhypotheses.     

Population genomics as a new tool for wildlife management

Admixture and introgression have varied effects on population viability and fitness. Admixture might be an important source of new alleles, particularly for small, geographically isolated populations. However, admixture might also cause outbreeding depression if populations are adapted to different ecological or climatic conditions. Because of the emerging use of translocation and admixture as a conservation and wildlife management strategy to reduce genetic load (termed genetic rescue), the possible effects of admixture have practical consequences ( Bouzat et al. 2009 ; Hedrick & Fredrickson 2010 ). Importantly, genetic load and local adaptation are properties of individual loci and epistatic interactions among loci rather than properties of genomes. Likewise, the outcome and consequences of genetic rescue depend on the fitness effects of individual introduced alleles. In this issue of Molecular Ecology, Miller et al. (2012) use model‐based, population genomic analyses to document locus‐specific effects of a recent genetic rescue in the bighorn sheep population within the National Bison Range wildlife refuge (NBR; Montana, USA). They find a subset of introduced alleles associated with increased fitness in NBR bighorn sheep, some of which experienced accelerated introgression following their introduction. These loci mark regions of the genome that could constitute the genetic basis of the successful NBR bighorn sheep genetic rescue. Although population genomic analyses are frequently used to study local adaptation and selection (e.g. Hohenlohe et al. 2010 ; Lawniczak et al. 2010 ), this study constitutes a novel application of this analytical framework for wildlife management. Moreover, the detailed demographic data available for the NBR bighorn sheep population provide a rare and powerful source of information and allow more robust population genomic inference than is often possible.     

Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers

We investigated the effect of development mode on the spatial and temporal population genetic structure of four littorinid gastropod species. Snails were collected from the same three sites on the west coast of Vancouver Island, Canada in 1997 and again in 2007. DNA sequences were obtained for one mitochondrial gene, cytochrome b ( Cyt b ), and for up to two nuclear genes, heat shock cognate 70 ( HSC70 ) and aminopeptidase N intron ( APN54 ). We found that the mean level of genetic diversity and long-term effective population sizes ( N _e) were significantly greater for two species, Littorina scutulata and L. plena , that had a planktotrophic larval stage than for two species, Littorina sitkana and L. subrotundata , that laid benthic egg masses which hatched directly into crawl-away juveniles. Predictably, two poorly dispersing species, L. sitkana and L. subrotundata , showed significant spatial genetic structure at an 11- to 65-km geographical scale that was not observed in the two planktotrophic species. Conversely, the two planktotrophic species had more temporal genetic structure over a 10-year interval than did the two direct-developing species and showed highly significant temporal structure for spatially pooled samples. The greater temporal genetic variation of the two planktotrophic species may have been caused by their high fecundity, high larval dispersal, and low but spatially correlated early survivorship. The sweepstakes-like reproductive success of the planktotrophic species could allow a few related females to populate hundreds of kilometres of coastline and may explain their substantially larger temporal genetic variance but lower spatial genetic variance relative to the direct-developing species.     

Strengths and potential pitfalls of hay transfer for ecological restoration revealed by RAD‐seq analysis in floodplain Arabis species

Achieving high intraspecific genetic diversity is a critical goal in ecological restoration as it increases the adaptive potential and long‐term resilience of populations. Thus, we investigated genetic diversity within and between pristine sites in a fossil floodplain and compared it to sites restored by hay transfer between 1997 and 2014. RAD‐seq genotyping revealed that the stenoecious floodplain species Arabis nemorensis is co‐occurring with individuals that, based on ploidy, ITS‐sequencing and morphology, probably belong to the close relative Arabis sagittata, which has a documented preference for dry calcareous grasslands but has not been reported in floodplain meadows. We show that hay transfer maintains genetic diversity for both species. Additionally, in A. sagittata, transfer from multiple genetically isolated pristine sites resulted in restored sites with increased diversity and admixed local genotypes. In A. nemorensis, transfer did not create novel admixture dynamics because genetic diversity between pristine sites was less differentiated. Thus, the effects of hay transfer on genetic diversity also depend on the genetic make‐up of the donor communities of each species, especially when local material is mixed. Our results demonstrate the efficiency of hay transfer for habitat restoration and emphasize the importance of prerestoration characterization of microgeographic patterns of intraspecific diversity of the community to guarantee that restoration practices reach their goal, that is maximize the adaptive potential of the entire restored plant community. Overlooking these patterns may alter the balance between species in the community. Additionally, our comparison of summary statistics obtained from de novo‐ and reference‐based RAD‐seq pipelines shows that the genomic impact of restoration can be reliably monitored in species lacking prior genomic knowledge.     

Advances in ecological genomics in forest trees and applications to genetic resources conservation and breeding

Forest trees are an unparalleled group of organisms in their combined ecological, economic and societal importance. With widespread distributions, predominantly random mating systems and large population sizes, most tree species harbour extensive genetic variation both within and among populations. At the same time, demographic processes associated with Pleistocene climate oscillations and land‐use change have affected contemporary range‐wide diversity and may impinge on the potential for future adaptation. Understanding how these adaptive and neutral processes have shaped the genomes of trees species is therefore central to their management and conservation. As for many other taxa, the advent of high‐throughput sequencing methods is expected to yield an understanding of the interplay between the genome and environment at a level of detail and depth not possible only a few years ago. An international conference entitled ‘Genomics and Forest Tree Genetics’ was held in May 2016, in Arcachon (France), and brought together forest geneticists with a wide range of research interests to disseminate recent efforts that leverage contemporary genomic tools to probe the population, quantitative and evolutionary genomics of trees. An important goal of the conference was to discuss how such data can be applied to both genome‐enabled breeding and the conservation of forest genetic resources under land use and climate change. Here, we report discoveries presented at the meeting and discuss how the ecological genomic toolkit can be used to address both basic and applied questions in tree biology.     

Spatial genetic patterns indicate mechanism and consequences of large carnivore cohabitation within development

Patterns of human development are shifting from concentrated housing toward sprawled housing intermixed with natural land cover, and wildlife species increasingly persist in close proximity to housing, roads, and other anthropogenic features. These associations can alter population dynamics and evolutionary trajectories. Large carnivores increasingly occupy urban peripheries, yet the ecological consequences for populations established entirely within urban and exurban landscapes are largely unknown. We applied a spatial and landscape genetics approach, using noninvasively collected genetic data, to identify differences in black bear spatial genetic patterns across a rural‐to‐urban gradient and quantify how development affects spatial genetic processes. We quantified differences in black bear dispersal, spatial genetic structure, and migration between differing levels of development within a population primarily occupying areas with >6 houses/km² in western Connecticut. Increased development disrupted spatial genetic structure, and we found an association between increased housing densities and longer dispersal. We also found evidence that roads limited gene flow among bears in more rural areas, yet had no effect among bears in more developed ones. These results suggest dispersal behavior is condition‐dependent and indicate the potential for landscapes intermixing development and natural land cover to facilitate shifts toward increased dispersal. These changes can affect patterns of range expansion and the phenotypic and genetic composition of surrounding populations. We found evidence that subpopulations occupying more developed landscapes may be sustained by male‐biased immigration, creating potentially detrimental demographic shifts.     

Phylogeography, genetic structure and population divergence time of cheetahs in Africa and Asia: evidence for long-term geographic isolates

The cheetah (Acinonyx jubatus) has been described as a species with low levels of genetic variation. This has been suggested to be the consequence of a demographic bottleneck 10 000–12 000 years ago (ya) and also led to the assumption that only small genetic differences exist between the described subspecies. However, analysing mitochondrial DNA and microsatellites in cheetah samples from most of the historic range of the species we found relatively deep phylogeographic breaks between some of the investigated populations, and most of the methods assessed divergence time estimates predating the postulated bottleneck. Mitochondrial DNA monophyly and overall levels of genetic differentiation support the distinctiveness of Northern‐East African cheetahs (Acinonyx jubatus soemmeringii). Moreover, combining archaeozoological and contemporary samples, we show that Asiatic cheetahs (Acinonyx jubatus venaticus) are unambiguously separated from African subspecies. Divergence time estimates from mitochondrial and nuclear data place the split between Asiatic and Southern African cheetahs (Acinonyx jubatus jubatus) at 32 000–67 000 ya using an average mammalian microsatellite mutation rate and at 4700–44 000 ya employing human microsatellite mutation rates. Cheetahs are vulnerable to extinction globally and critically endangered in their Asiatic range, where the last 70–110 individuals survive only in Iran. We demonstrate that these extant Iranian cheetahs are an autochthonous monophyletic population and the last representatives of the Asiatic subspecies A. j. venaticus. We advocate that conservation strategies should consider the uncovered independent evolutionary histories of Asiatic and African cheetahs, as well as among some African subspecies. This would facilitate the dual conservation priorities of maintaining locally adapted ecotypes and genetic diversity.     

Evaluating methods to visualize patterns of genetic differentiation on a landscape

With advances in sequencing technology, research in the field of landscape genetics can now be conducted at unprecedented spatial and genomic scales. This has been especially evident when using sequence data to visualize patterns of genetic differentiation across a landscape due to demographic history, including changes in migration. Two recent model‐based visualization methods that can highlight unusual patterns of genetic differentiation across a landscape, SpaceMix and EEMS, are increasingly used. While SpaceMix's model can infer long‐distance migration, EEMS’ model is more sensitive to short‐distance changes in genetic differentiation, and it is unclear how these differences may affect their results in various situations. Here, we compare SpaceMix and EEMS side by side using landscape genetics simulations representing different migration scenarios. While both methods excel when patterns of simulated migration closely match their underlying models, they can produce either un‐intuitive or misleading results when the simulated migration patterns match their models less well, and this may be difficult to assess in empirical data sets. We also introduce unbundled principal components (un‐PC), a fast, model‐free method to visualize patterns of genetic differentiation by combining principal components analysis (PCA), which is already used in many landscape genetics studies, with the locations of sampled individuals. Un‐PC has characteristics of both SpaceMix and EEMS and works well with simulated and empirical data. Finally, we introduce msLandscape, a collection of tools that streamline the creation of customizable landscape‐scale simulations using the popular coalescent simulator ms and conversion of the simulated data for use with un‐PC, SpaceMix and EEMS.     

Phylogeography, genetic structure and diversity in the endangered bearded vulture (Gypaetus barbatus, L) as revealed by mitochondrial DNA

Bearded vulture populations in the Western Palearctic have experienced a severe decline during the last two centuries that has led to the near extinction of the species in Europe. In this study we analyse the sequence variation at the mitochondrial control region throughout the species range to infer its recent evolutionary history and to evaluate the current genetic status of the species. This study became possible through the extensive use of museum specimens to study populations now extinct. Phylogenetic analysis revealed the existence of two divergent mitochondrial lineages, lineage A occurring mainly in Western European populations and lineage B in African, Eastern European and Central Asian populations. The relative frequencies of haplotypes belonging to each lineage in the different populations show a steep East-West clinal distribution with maximal mixture of the two lineages in the Alps and Greece populations. A genealogical signature for population growth was found for lineage B, but not for lineage A; futhermore the Clade B haplotypes in western populations and clade A haplo-types in eastern populations are recently derived, as revealed by their peripheral location in median-joining haplotype networks. This phylogeographical pattern suggests allopatric differentiation of the two lineages in separate Mediterranean and African or Asian glacial refugia, followed by range expansion from the latter leading to two secondary contact suture zones in Central Europe and North Africa. High levels of among-population differentiation were observed, although these were not correlated with geographical distance. Due to the marked genetic structure, extinction of Central European populations in the last century re-sulted in the loss of a major portion of the genetic diversity of the species. We also found direct evidence for the effect of drift altering the genetic composition of the remnant Pyrenean population after the demographic bottleneck of the last century. Our results argue for the management of the species as a single population, given the apparent ecological exchangeability of extant stocks, and support the ongoing reintroduction of mixed ancestry birds in the Alps and planned reintroductions in Southern Spain.     

Combining population genomics and ecological niche modeling to assess taxon limits between Carex jemtlandica and C. lepidocarpa

Carex section Ceratocystis (Cyperaceae) is a group of recently evolved plant species, in which hybridization is frequent, introgression is documented, taxonomy is complex, and morphological boundaries are vague. Within this section, a unified taxonomic treatment of the Carex jemtlandica–Carex lepidocarpa species complex does not exist, and Norway may currently be the sole country accepting species rank for both. Carex jemtlandica is mainly confined to Fennoscandia and is thus a Fennoscandian conservation responsibility. This motivated us to test the principal hypothesis that both C. jemtlandica and C. lepidocarpa represent evolutionary significant units, and that both deserve their current recognition at species level. We investigated their evolutionary distinctiveness in Norway,using restriction site-associated DNA sequencing and ecological niche modeling. Our genomic results reveal two genetic clusters, largely corresponding to C. jemtlandica and C. lepidocarpa that also remain distinct in sympatry, despite clear indications of ongoing hybridization and introgression. The ecological niche modeling suggests that they occupy different environmental niches. Jointly, our results clearly show that C. jemtlandica and C. lepidocarpa represent separately evolving entities that should qualify recognition as evolutionary significant units. Given the high level of introgression compared to other hybridizing species pairs in Carex we recommend treating C. jemtlandica as a subspecies of C. lepidocarpa.     

The future is now: Amplicon sequencing and sequence capture usher in the conservation genomics era

The genomics revolution has initiated a new era of population genetics where genome‐wide data are frequently used to understand complex patterns of population structure and selection. However, the application of genomic tools to inform management and conservation has been somewhat rare outside a few well studied species. Fortunately, two recently developed approaches, amplicon sequencing and sequence capture, have the potential to significantly advance the field of conservation genomics. Here, amplicon sequencing refers to highly multiplexed PCR followed by high‐throughput sequencing (e.g., GTseq), and sequence capture refers to using capture probes to isolate loci from reduced‐representation libraries (e.g., Rapture). Both approaches allow sequencing of thousands of individuals at relatively low costs, do not require any specialized equipment for library preparation, and generate data that can be analyzed without sophisticated computational infrastructure. Here, we discuss the advantages and disadvantages of each method and provide a decision framework for geneticists who are looking to integrate these methods into their research programme. While it will always be important to consider the specifics of the biological question and system, we believe that amplicon sequencing is best suited for projects aiming to genotype <500 loci on many individuals (>1,500) or for species where continued monitoring is anticipated (e.g., long‐term pedigrees). Sequence capture, on the other hand, is best applied to projects including fewer individuals or where >500 loci are required. Both of these techniques should smooth the transition from traditional genetic techniques to genomics, helping to usher in the conservation genomics era.     

Phylogeography and population genetic structure of the European roe deer in Switzerland following recent recolonization

In the early 1800s, the European roe deer (Capreolus capreolus) was probably extirpated from Switzerland, due to overhunting and deforestation. After a federal law was enacted in 1875 to protect lactating females and young, and limiting the hunting season, the roe deer successfully recovered and recolonized Switzerland. In this study, we use mitochondrial DNA and nuclear DNA markers to investigate the recolonization and assess contemporary genetic structure in relation to broad topographic features, in order to understand underlying ecological processes, inform future roe deer management strategies, and explore the opportunity for development of forensic traceability tools. The results concerning the recolonization origin support natural, multidirectional immigration from neighboring countries. We further demonstrate that there is evidence of weak genetic differentiation within Switzerland among topographic regions. Finally, we conclude that the genetic data support the recognition of a single roe deer management unit within Switzerland, within which there is a potential for broad‐scale geographic origin assignment using nuclear markers to support law enforcement.     

Four cleaved amplified polymorphic sequence (CAPS) markers for the detection of the Juglans ailantifolia chloroplast in putatively native J. cinerea populations

Hybridization between butternut (Juglans cinerea), a forest tree native to eastern North America, and Japanese walnut (J. ailantifolia), a tree tolerant to the lethal fungal disease butternut canker, casts doubt on the genetic identity of the remaining butternuts. We report a diagnostic test to distinguish the J. cinerea chloroplast from the J. ailantifolia chloroplast using cleaved amplified polymorphic sequences resolvable in 1.5% agarose gels. J. ailantifolia maternal ancestry in naturally regenerated stands provides a site selection criterion for studies of introgression dynamics when the non-native parent and the hybrids tolerate a disease to which the native species is susceptible.     

Social kin associations and genetic structuring of striped dolphin populations (Stenella coeruleoalba) in the Mediterranean Sea

We investigated hierarchical patterns of genetic subdivision, and assessed kinship within and between social groups of striped dolphins (Stenella coeruleoalba) in the Tyrrhenian Sea. A total of 165 samples were analysed at eight microsatellite DNA loci, including outgroup samples from the Adriatic, Scotland and Spain for population-level comparisons. We found population genetic structure within the Mediterranean basin, including small but significant differentiation between the Adriatic and Tyrrhenian Seas (FST=0.0047, P=0.008), and between putative 'inshore' and 'offshore' (FST=0.0217, P=0.005) populations in the Tyrrhenian Sea. Assessment of kinship within and among 12 association groups showed higher average kinship for females within than between groups, and smaller groups showed higher average kinship. Comparisons of relatedness for both sexes showed a significant difference between males and females, with females more likely to associate with adult kin. Together these data emphasize the importance of the social cohesion of kin in small groups to the structuring of striped dolphin populations in this environment.     

Asymmetric oceanographic processes mediate connectivity and population genetic structure,as revealed by RADseq,in a highly dispersive marine invertebrate (Parastichopus californicus)

Marine populations are typically characterized by weak genetic differentiation due to the potential for long‐distance dispersal favouring high levels of gene flow. However, strong directional advection of water masses or retentive hydrodynamic forces can influence the degree of genetic exchange among marine populations. To determine the oceanographic drivers of genetic structure in a highly dispersive marine invertebrate, the giant California sea cucumber (Parastichopus californicus), we first tested for the presence of genetic discontinuities along the coast of North America in the northeastern Pacific Ocean. Then, we tested two hypotheses regarding spatial processes influencing population structure: (i) isolation by distance (IBD: genetic structure is explained by geographic distance) and (ii) isolation by resistance (IBR: genetic structure is driven by ocean circulation). Using RADseq, we genotyped 717 individuals from 24 sampling locations across 2,719 neutral SNPs to assess the degree of population differentiation and integrated estimates of genetic variation with inferred connectivity probabilities from a biophysical model of larval dispersal mediated by ocean currents. We identified two clusters separating north and south regions, as well as significant, albeit weak, substructure within regions (F_ST = 0.002, p = .001). After modelling the asymmetric nature of ocean currents, we demonstrated that local oceanography (IBR) was a better predictor of genetic variation (R² = .49) than geographic distance (IBD) (R² = .18), and directional processes played an important role in shaping fine‐scale structure. Our study contributes to the growing body of literature identifying significant population structure in marine systems and has important implications for the spatial management of P. californicus and other exploited marine species.     

Spatial and temporal genetic structure in a hybrid cordgrass invasion

Invasive hybrids and their spread dynamics pose unique opportunities to study evolutionary processes. Invasive hybrids of native Spartina foliosa and introduced S. alterniflora have expanded throughout San Francisco Bay intertidal habitats within the past 35 years by deliberate plantation and seeds floating on the tide. Our goals were to assess spatial and temporal scales of genetic structure in Spartina hybrid populations within the context of colonization history. We genotyped adult and seedling Spartina using 17 microsatellite loci and mapped their locations in three populations. All sampled seedlings were hybrids. Bayesian ordination analysis distinguished hybrid populations from parent species, clearly separated the population that originated by plantation from populations that originated naturally by seed and aligned most seedlings within each population. Population genetic structure estimated by analysis of molecular variance was substantial (F_ST=0.21). Temporal genetic structure among age classes varied highly between populations. At one population, the divergence between adults and 2004 seedlings was low (F_ST=0.02) whereas at another population this divergence was high (F_ST=0.26). This latter result was consistent with local recruitment of self-fertilized seed produced by only a few parental plants. We found fine-scale spatial genetic structure at distances less than ∼200 m, further supporting local seed and/or pollen dispersal. We posit a few self-fertile plants dominating local recruitment created substantial spatial genetic structure despite initial long-distance, human dispersal of hybrid Spartina through San Francisco Bay. Fine-scale genetic structure may more strongly develop when local recruits are dominated by the offspring of a few self-fertile plants.     

Rarity and genetic diversity in Indo-Pacific Acropora corals

Among various potential consequences of rarity is genetic erosion. Neutral genetic theory predicts that rare species will have lower genetic diversity than common species. To examine the association between genetic diversity and rarity, variation at eight DNA microsatellite markers was documented for 14 Acropora species that display different patterns of distribution and abundance in the Indo-Pacific Ocean. Our results show that the relationship between rarity and genetic diversity is not a positive linear association because, contrary to expectations, some rare species are genetically diverse and some populations of common species are genetically depleted. Our data suggest that inbreeding is the most likely mechanism of genetic depletion in both rare and common corals, and that hybridization is the most likely explanation for higher than expected levels of genetic diversity in rare species. A significant hypothesis generated from our study with direct conservation implications is that as a group, Acropora corals have lower genetic diversity at neutral microsatellite loci than may be expected from their taxonomic diversity, and this may suggest a heightened susceptibility to environmental change. This hypothesis requires validation based on genetic diversity estimates derived from a large portion of the genome.     

Extreme genetic differentiation among the remnant populations of marble trout (Salmo marmoratus) in Slovenia

Populations of the marble trout (Salmo marmoratus) have declined critically due to introgression by brown trout (Salmo trutta) strains. In order to define strategies for long-term conservation, we examined the genetic structure of the 8 known pure populations using 15 microsatellite loci. The analyses reveal extraordinarily strong genetic differentiation among populations separated by < 15 km, and extremely low levels of intrapopulation genetic variability. As natural recolonization seems highly unlikely, appropriate management and conservation strategies should comprise the reintroduction of pure populations from mixed stocks (translocation) to avoid further loss of genetic diversity.     

Genetic consequences of population expansions and contractions in the common hippopotamus (Hippopotamus amphibius) since the Late Pleistocene

Over the past two decades, an increasing amount of phylogeographic work has substantially improved our understanding of African biogeography, in particular the role played by Pleistocene pluvial–drought cycles on terrestrial vertebrates. However, still little is known on the evolutionary history of semi‐aquatic animals, which faced tremendous challenges imposed by unpredictable availability of water resources. In this study, we investigate the Late Pleistocene history of the common hippopotamus (Hippopotamus amphibius), using mitochondrial and nuclear DNA sequence variation and range‐wide sampling. We documented a global demographic and spatial expansion approximately 0.1–0.3 Myr ago, most likely associated with an episode of massive drainage overflow. These events presumably enabled a historical continent‐wide gene flow among hippopotamus populations, and hence, no clear continental‐scale genetic structuring remains. Nevertheless, present‐day hippopotamus populations are genetically disconnected, probably as a result of the mid‐Holocene aridification and contemporary anthropogenic pressures. This unique pattern contrasts with the biogeographic paradigms established for savannah‐adapted ungulate mammals and should be further investigated in other water‐associated taxa. Our study has important consequences for the conservation of the hippo, an emblematic but threatened species that requires specific protection to curtail its long‐term decline.