Y‐chromosome and mtDNA variation confirms independent domestications and directional hybridization in South American camelids

Investigations of genetic diversity and domestication in South American camelids (SAC) have relied on autosomal microsatellite and maternally‐inherited mitochondrial data. We present the first integrated analysis of domestic and wild SAC combining male and female sex‐specific markers (male specific Y‐chromosome and female‐specific mtDNA sequence variation) to assess: (i) hypotheses about the origin of domestic camelids, (ii) directionality of introgression among domestic and/or wild taxa as evidence of hybridization and (iii) currently recognized subspecies patterns. Three male‐specific Y‐chromosome markers and control region sequences of mitochondrial DNA are studied here. Although no sequence variation was found in SRY and ZFY, there were seven variable sites in DBY generating five haplotypes on the Y‐chromosome. The haplotype network showed clear separation between haplogroups of guanaco–llama and vicuña–alpaca, indicating two genetically distinct patrilineages with near absence of shared haplotypes between guanacos and vicuñas. Although we document some examples of directional hybridization, the patterns strongly support the hypothesis that llama (Lama glama) is derived from guanaco (Lama guanicoe) and the alpaca (Vicugna pacos) from vicuña (Vicugna vicugna). Within male guanacos we identified a haplogroup formed by three haplotypes with different geographical distributions, the northernmost of which (Peru and northern Chile) was also observed in llamas, supporting the commonly held hypothesis that llamas were domesticated from the northernmost populations of guanacos (L. g. cacilensis). Southern guanacos shared the other two haplotypes. A second haplogroup, consisting of two haplotypes, was mostly present in vicuñas and alpacas. However, Y‐chromosome variation did not distinguish the two subspecies of vicuñas.     

Contrasting genetic diversity patterns in two sister kelp species co‐distributed along the coast of Brittany,France

We investigated patterns of genetic structure in two sister kelp species to explore how distribution width along the shore, zonation, latitudinal distribution and historical factors contribute to contrasting patterns of genetic diversity. We implemented a hierarchical sampling scheme to compare patterns of genetic diversity and structure in these two kelp species co‐distributed along the coasts of Brittany (France) using a total of 12 microsatellites, nine for Laminaria hyperborea and 11 for Laminaria digitata, of which eight amplified in both species. The genetic diversity and connectivity of L. hyperborea populations were greater than those of L. digitata populations in accordance with the larger cross‐shore distribution width along the coast and the greater depth occupied by L. hyperborea populations in contrast to L. digitata populations. In addition, marginal populations showed reduced genetic diversity and connectivity, which erased isolation‐by‐distance patterns in both species. As L. digitata encounters its southern range limit in southern Brittany (SBr) while L. hyperborea extends down to mid‐Portugal, it was possible to distinguish the effect of habitat continuity from range edge effects. We found that L. digitata did not harbour high regional diversity at its southern edge, as expected in a typical rear edge, suggesting that refuges from the last glacial maximum for L. digitata were probably not located in SBr, but most likely further north. For both species, the highest levels of genetic diversity were found in the Iroise Sea and Morlaix Bay, the two regions in which they are being currently harvested. Preserving genetic diversity of these two foundation species in these areas should, thus, be a priority for the management of this resource in Brittany.     

Foraging and vigilance time allocation in a guanaco (<Emphasis Type="Italic">Lama guanicoe</Emphasis>) population reintroduced in Quebrada del Condorito National Park (Córdoba,Argentina)

In reintroduction projects, ethology studies play a significant role in evaluating the behaviour of the individuals in habitats where they are reintroduced. We studied foraging and vigilance time allocation of a guanaco (Lama guanicoe) population reintroduced in Quebrada del Condorito National Park (QCNP), in the central mountains of Córdoba, Argentina. On average, individuals showed a higher proportion of time invested in vigilance and a lower proportion of time invested in foraging than a previously studied guanaco population belonging to the same ecological region as the source population, suggesting that at the time of this study, the reintroduced population was not fully adapted to the new habitat or suffered from an increased predation pressure. On the other hand, as expected for the species, throughout the study period, males allocated more time to vigilance than females, both sexes increasing vigilance during the reproductive period, and females increasing foraging time allocation during the post-reproductive period. Taking into account that further reinforcement to the existing population is planned, the present results may contribute to the elaboration of management strategies aimed at the successful establishment of guanaco in QCNP.     

The return of the frogs: The importance of habitat refugia in maintaining diversity during a disease outbreak

Recent decades have seen the emergence and spread of numerous infectious diseases, often with severe negative consequences for wildlife populations. Nevertheless, many populations survive the initial outbreaks, and even undergo recoveries. Unfortunately, the long‐term effects of these outbreaks on host population genetics are poorly understood; to increase this understanding, we examined the population genetics of two species of rainforest frogs (Litoria nannotis and Litoria serrata) that have largely recovered from a chytridiomycosis outbreak at two national parks in the Wet Tropics of northern Australia. At the wetter, northern park there was little evidence of decreased genetic diversity in either species, and all of the sampled sites had high minor allele frequencies (mean MAF = 0.230–0.235), high heterozygosity (0.318–0.325), and few monomorphic markers (1.4%–4.0%); however, some recovered L. nannotis populations had low N_e values (59.3–683.8) compared to populations that did not decline during the outbreak (1,537.4–1,756.5). At the drier, southern park, both species exhibited lower diversity (mean MAF = 0.084–0.180; heterozygosity = 0.126–0.257; monomorphic markers = 3.7%–43.5%; N_e = 18.4–676.1). The diversity patterns in this park matched habitat patterns, with both species having higher diversity levels and fewer closely related individuals at sites with higher quality habitat. These patterns were more pronounced for L. nannotis, which has lower dispersal rates than L. serrata. These results suggest that refugia with high quality habitat are important for retaining genetic diversity during disease outbreaks, and that gene flow following disease outbreaks is important for re‐establishing diversity in populations where it was reduced.     

High levels of population subdivision in a morphologically conserved Mediterranean toad (Alytes cisternasii) result from recent,multiple refugia: evidence from mtDNA,microsatellites and nuclear genealogies

Pleistocene glaciations often resulted in differentiation of taxa in southern European peninsulas, producing the high levels of endemism characteristic of these regions (e.g. the Iberian Peninsula). Despite their small ranges, endemic species often exhibit high levels of intraspecific differentiation as a result of a complex evolutionary history dominated by successive cycles of fragmentation, expansion and subsequent admixture of populations. Most evidence so far has come from the study of species with an Atlantic distribution in northwestern Iberia, and taxa restricted to Mediterranean‐type habitats remain poorly studied. The Iberian Midwife toad (Alytes cisternasii) is a morphologically conserved species endemic to southwestern and central Iberia and a typical inhabitant of Mediterranean habitats. Applying highly variable genetic markers from both mitochondrial and nuclear genomes to samples collected across the species’ range, we found evidence of high population subdivision within A. cisternasii. Mitochondrial haplotypes and microsatellites show geographically concordant patterns of genetic diversity, suggesting population fragmentation into several refugia during Pleistocene glaciations followed by subsequent events of geographical and demographic expansions with secondary contact. In addition, the absence of variation at the nuclear β‐fibint7 and Ppp3caint4 gene fragments suggests that populations of A. cisternasii have been recurrently affected by episodes of extinction and recolonization, and that documented patterns of population subdivision are the outcome of recent and multiple refugia. We discuss the evolutionary history of the species with particular interest in the increasing relevance of Mediterranean refugia for the survival of genetically differentiated populations during the Pleistocene glaciations as revealed by studies in co‐distributed taxa.     

Contrasting geographic structure in evolutionarily divergent Lake Tanganyika catfishes

Geographic isolation is suggested to be among the most important processes in the generation of cichlid fish diversity in East Africa's Great Lakes, both through isolation by distance and fluctuating connectivity caused by changing lake levels. However, even broad scale phylogeographic patterns are currently unknown in many non‐cichlid littoral taxa from these systems. To begin to address this, we generated restriction‐site‐associated DNA sequence (RADseq) data to investigate phylogeographic structure throughout Lake Tanganyika (LT) in two broadly sympatric rocky shore catfish species from independent evolutionary radiations with differing behaviors: the mouthbrooding claroteine, Lophiobagrus cyclurus, and the brood‐parasite mochokid, Synodontis multipunctatus. Our results indicated contrasting patterns between these species, with strong lake‐wide phylogeographic signal in L. cyclurus including a deep divergence between the northern and southern lake basins. Further structuring of these populations was observed across a heterogeneous habitat over much smaller distances. Strong population growth was observed in L. cyclurus sampled from shallow shorelines, suggesting population growth associated with the colonization of new habitats following lake‐level rises. Conversely, S. multipunctatus, which occupies a broader depth range, showed little phylogeographic structure and lower rates of population growth. Our findings suggest that isolation by distance and/or habitat barriers may play a role in the divergence of non‐cichlid fishes in LT, but this effect varies by species.     

Chironomus riparius (Diptera) genome sequencing reveals the impact of minisatellite transposable elements on population divergence

Active transposable elements (TEs) may result in divergent genomic insertion and abundance patterns among conspecific populations. Upon secondary contact, such divergent genetic backgrounds can theoretically give rise to classical Dobzhansky–Muller incompatibilities (DMI), thus contributing to the evolution of endogenous genetic barriers and eventually causing population divergence. We investigated differential TE abundance among conspecific populations of the nonbiting midge Chironomus riparius and evaluated their potential role in causing endogenous genetic incompatibilities between these populations. We focussed on a Chironomus‐specific TE, the minisatellite‐like Cla‐element, whose activity is associated with speciation in the genus. Using a newly generated and annotated draft genome for a genomic study with five natural C. riparius populations, we found highly population‐specific TE insertion patterns with many private insertions. A significant correlation of the pairwise F_ST estimated from genomewide single‐nucleotide polymorphisms (SNPs) and the F_ST estimated from TEs is consistent with drift as the major force driving TE population differentiation. However, the significantly higher Cla‐element F_ST level due to a high proportion of differentially fixed Cla‐element insertions also indicates selection against segregating (i.e. heterozygous) insertions. With reciprocal crossing experiments and fluorescent in situ hybridization of Cla‐elements to polytene chromosomes, we documented phenotypic effects on female fertility and chromosomal mispairings. We propose that the inferred negative selection on heterozygous Cla‐element insertions may cause endogenous genetic barriers and therefore acts as DMI among C. riparius populations. The intrinsic genomic turnover exerted by TEs may thus have a direct impact on population divergence that is operationally different from drift and local adaptation.     

Migratory behaviour shapes spatial genetic structure of cyprinid fishes within the Lake Malawi catchment

• Genetic differences among freshwater fish populations are dependent on life‐history characteristics of the species, including the range of adult dispersal and the extent of homing to natal breeding grounds. However, the effects of variation in such characteristics on population genetic connectivity are rarely studied comparatively among closely related species.
• We studied population genetic structure within three congeneric cyprinid species from the Lake Malawi catchment that differ substantially in life‐history traits and conservation status, using a combination of microsatellite and mitochondrial DNA markers. Mpasa (Opsaridium microlepis) is a large (70 cm total length) migratory species that spawns in rivers, but as an adult is exclusively known from the main lake body. Sanjika (Opsaridium microcephalum), is a medium size (30 cm total length) species that exists in lake breeding, river‐lake migratory and apparently landlocked populations. Dwarf sanjika (Opsaridium tweddleorum) is a small non‐migratory species (15 cm total length) that persists in small tributaries surrounding the main lake and adjoining rivers.
• The results revealed striking differences among the three species in spatial genetic structuring. The river‐lake migratory mpasa showed only weak yet significant population genetic structure within the main Lake Malawi catchment, suggesting that there is no strong natal homing. The habitat‐generalist sanjika showed only weak spatial genetic differentiation at microsatellite loci within the Lake Malawi catchment, but moderate structure in mitochondrial DNA, potentially reflecting male‐biased dispersal. The river‐restricted dwarf sanjika showed strong genetic structure in both microsatellite and mitochondrial DNA, suggesting strictly limited dispersal at both adult and juvenile stages.
• We conclude that contrasting migration life histories have resulted in dramatically different patterns of population genetic structure among these congeneric species. The observed patterns demonstrate how divergent life‐history evolution may strongly influence broader patterns of population genetic connectivity in freshwater fish, with consequences for management and conservation. Specifically the results suggesting gene flow among Lake Malawi populations of mpasa, an IUCN red‐listed ‘Endangered’ species endemic to the lake catchment, imply that conservation initiatives operating at both local and catchment scales are needed to reverse local population decline.

     

Range‐wide population genetic structure of the Caribbean sea fan coral,Gorgonia ventalina

The population structure of benthic marine organisms is of central relevance to the conservation and management of these often threatened species, as well as to the accurate understanding of their ecological and evolutionary dynamics. A growing body of evidence suggests that marine populations can be structured over short distances despite theoretically high dispersal potential. Yet the proposed mechanisms governing this structure vary, and existing empirical population genetic evidence is of insufficient taxonomic and geographic scope to allow for strong general inferences. Here, we describe the range‐wide population genetic structure of an ecologically important Caribbean octocoral, Gorgonia ventalina. Genetic differentiation was positively correlated with geographic distance and negatively correlated with oceanographically modelled dispersal probability throughout the range. Although we observed admixture across hundreds of kilometres, estimated dispersal was low, and populations were differentiated across distances <2 km. These results suggest that populations of G. ventalina may be evolutionarily coupled via gene flow but are largely demographically independent. Observed patterns of differentiation corroborate biogeographic breaks found in other taxa (e.g. an east/west divide near Puerto Rico), and also identify population divides not discussed in previous studies (e.g. the Yucatan Channel). High genotypic diversity and absence of clonemates indicate that sex is the primary reproductive mode for G. ventalina. A comparative analysis of the population structure of G. ventalina and its dinoflagellate symbiont, Symbiodinium, indicates that the dispersal of these symbiotic partners is not coupled, and symbiont transmission occurs horizontally.     

Congruent population genetic structure but differing depths of divergence for three alpine stoneflies with similar ecology and geographic distributions

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Low genetic variability and strong differentiation among isolated populations of the rare steppe grass Stipa capillata L. in Central Europe

Stipa capillata L. (Poaceae) is a rare grassland species in Central Europe that is thought to have once been widespread in post‐glacial times. Such relict species are expected to show low genetic diversity within populations and high genetic differentiation between populations due to bottlenecks, long‐term isolation and ongoing habitat fragmentation. These patterns should be particularly pronounced in selfing species. We analysed patterns of random amplified polymorphic DNA (RAPD) variation in the facultatively cleistogamous S. capillata to examine whether genetic diversity is associated with population size, and to draw initial conclusions on the migration history of this species in Central Europe. We analysed 31 S. capillata populations distributed in northeastern, central and western Germany, Switzerland and Slovakia. Estimates of genetic diversity at the population level were low and not related to population size. Among all populations, extraordinarily high levels of genetic differentiation (amova : φ_ST = 0.86; Bayesian analysis: θ^B = 0.758) and isolation‐by‐distance were detected. Hierarchical amova indicated that most of the variability was partitioned among geographic regions (59%), or among populations between regions when the genetically distinct Slovakian populations were excluded. These findings are supported by results of a multivariate ordination analysis. We also found two different groups in an UPGMA cluster analysis: one that contained the populations from Slovakia, and the other that combined the populations from Germany and Switzerland. Our findings imply that S. capillata is indeed a relict species that experienced strong bottlenecks in Central Europe, enhanced by isolation and selfing. Most likely, populations in Slovakia were not the main genetic source for the post‐glacial colonization of Central Europe.     

Late Quaternary climatic vegetational shifts in an ecological transition zone of northern Madagascar: insights from genetic analyses of two endemic rodent species

The Loky‐Manambato region, located in northern Madagascar, is a biotically rich contact zone between different forest biomes. Local current forest cover is composed of both humid and dry formations, which show elevational stratification. A recent phylogeographical study of a regional dry forest rodent, Eliurus carletoni (subfamily Nesomyinae), found genetic evidence of forest contractions between 18 750 and 7500 years BP, which based on extrapolation of the pollen subfossil record, was thought to be associated with an expansion of local humid forests. Herein, we conduct a genetic test of this hypothesis and focused on populations on two neighbouring massifs of forest‐dependent rodent species, one associated with low‐elevation dry forests (E. carletoni) and the other with higher elevation humid forests (Eliurus tanala). Using mitochondrial markers and a combination of traditional and coalescent‐based phylogeographical, historical demographic and population genetic methods, we found evidence of historical connections between populations of E. tanala. Adjacent populations of E. carletoni and E. tanala exhibit opposite historical demographic patterns, and for both, evidence suggests that historical demographic events occurred within the last 25 000 years BP. These findings strongly support the proposed late Quaternary shifts in the floristic composition of the Loky‐Manambato region.     

Integrating multiple lines of evidence to better understand the evolutionary divergence of humpback dolphins along their entire distribution range: a new dolphin species in Australian waters?

The conservation of humpback dolphins, distributed in coastal waters of the Indo‐West Pacific and eastern Atlantic Oceans, has been hindered by a lack of understanding about the number of species in the genus (Sousa) and their population structure. To address this issue, we present a combined analysis of genetic and morphologic data collected from beach‐cast, remote‐biopsied and museum specimens from throughout the known Sousa range. We extracted genetic sequence data from 235 samples from extant populations and explored the mitochondrial control region and four nuclear introns through phylogenetic, population‐level and population aggregation frameworks. In addition, 180 cranial specimens from the same geographical regions allowed comparisons of 24 morphological characters through multivariate analyses. The genetic and morphological data showed significant and concordant patterns of geographical segregation, which are typical for the kind of demographic isolation displayed by species units, across the Sousa genus distribution range. Based on our combined genetic and morphological analyses, there is convincing evidence for at least four species within the genus (S. teuszii in the Atlantic off West Africa, S. plumbea in the central and western Indian Ocean, S. chinensis in the eastern Indian and West Pacific Oceans, and a new as‐yet‐unnamed species off northern Australia).     

Isolation and characterization of 10 polymorphic dinucleotide microsatellite markers for llama and guanaco

We isolated and characterized five polymorphic dinucleotide microsatellite markers from llama (Lama glama) and five from guanaco (Lama guanicoe). All loci were assayed on wild llamas and guanacos from Argentina, as all of the primers were able to amplify in both species.     

Genomics and museum specimens

Nearly 25 years ago, Allan Wilson and colleagues isolated DNA sequences from museum specimens of kangaroo rats (Dipodomys panamintinus) and compared these sequences with those from freshly collected animals (Thomas et al. 1990 ). The museum specimens had been collected up to 78 years earlier, so the two samples provided a direct temporal comparison of patterns of genetic variation. This was not the first time DNA sequences had been isolated from preserved material, but it was the first time it had been carried out with a population sample. Population geneticists often try to make inferences about the influence of historical processes such as selection, drift, mutation and migration on patterns of genetic variation in the present. The work of Wilson and colleagues was important in part because it suggested a way in which population geneticists could actually study genetic change in natural populations through time, much the same way that experimentalists can do with artificial populations in the laboratory. Indeed, the work of Thomas et al. ( 1990 ) spawned dozens of studies in which museum specimens were used to compare historical and present‐day genetic diversity (reviewed in Wandeler et al. 2007 ). All of these studies, however, were limited by the same fundamental problem: old DNA is degraded into short fragments. As a consequence, these studies mostly involved PCR amplification of short templates, usually short stretches of mitochondrial DNA or microsatellites. In this issue, Bi et al. ( 2013 ) report a breakthrough that should open the door to studies of genomic variation in museum specimens. They used target enrichment (exon capture) and next‐generation (Illumina) sequencing to compare patterns of genetic variation in historic and present‐day population samples of alpine chipmunks (Tamias alpinus) (Fig. 1). The historic samples came from specimens collected in 1915, so the temporal span of this comparison is nearly 100 years.     

Limited cross‐species microsatellite amplification and the isolation and characterization of new microsatellite markers for the greater stick‐nest rat (Leporillus conditor)

The greater stick‐nest rat (Leporillus conditor) is a conilurid rodent whose recent history provides an opportunity to examine genetic changes in reintroduced populations. We trialled 63 known microsatellite primers from Rattus rattus and Mus musculus in L. conditor. Three primer pairs produced polymorphic loci (number of alleles = 2–3, mean, H_E = 0.42). Subsequently, we isolated and characterized 12 novel polymorphic microsatellites (mean number of alleles = 5–16, mean H_E = 0.76) from L. conditor from genomic libraries for use in population genetic studies.     

Polyploid origin,genetic diversity and population structure in the tetraploid sea lavender <Emphasis Type="Italic">Limonium narbonense</Emphasis> Miller (Plumbaginaceae) from eastern Spain

Limonium narbonense Miller is a fertile tetraploid species with a sporophytic self-incompatibility system. This sea lavender is found in coastal salt marshes which have been under intense human pressure during the past decades resulting in significant habitat fragmentation. Eleven microsatellite loci specifically designed for this species were amplified in 135 individuals from five populations. These markers were used to investigate the polyploid nature, the levels of genetic diversity and population structure in this species. L. narbonense showed high levels of genetic diversity (A = 7.82, P = 100% H _T = 0.446), consistent with its likely autotetraploid origin revealed in this study and obligate outcrossing breeding system. Inbreeding (F _IS) values were low in the three southern populations (mean F _IS = 0.062), and higher in the northern populations (mean F _IS = 0.184). Bayesian analysis of population structure revealed that populations could be grouped into two genetic clusters, one including three southern populations and the other the two northernmost ones. Individuals from the two northernmost populations showed higher admixture of the two genetic clusters than individuals from the three southern ones. A thorough analysis of microsatellite electrophoretic patterns suggests an autotetraploid origin for L. narbonense. The genetic structure revealed in this study is attributed to a recent migration from the southern area. This result suggests a net gene flow from the south to the north, likely facilitated by migratory movements of birds visiting the temporary flooded ponds occupied by L. narbonense.     

Do plant populations on distinct inselbergs talk to each other? A case study of genetic connectivity of a bromeliad species in an Ocbil landscape

Here, we explore the historical and contemporaneous patterns of connectivity among Encholirium horridum populations located on granitic inselbergs in an Ocbil landscape within the Brazilian Atlantic Forest, using both nuclear and chloroplast microsatellite markers. Beyond to assess the E. horridum population genetic structure, we built species distribution models across four periods (current conditions, mid‐Holocene, Last Glacial Maximum [LGM], and Last Interglacial) and inferred putative dispersal corridors using a least‐cost path analysis to elucidate biogeographic patterns. Overall, high and significant genetic divergence was estimated among populations for both nuclear and plastid DNA (Φ_ST(n) = 0.463 and Φ_ST(plastid) = 0.961, respectively, p < .001). For nuclear genome, almost total absence of genetic admixture among populations and very low migration rates were evident, corroborating with the very low estimates of immigration and emigration rates observed among E. horridum populations. Based on the cpDNA results, putative dispersal routes in Sugar Loaf Land across cycles of climatic fluctuations in the Quaternary period revealed that the populations’ connectivity changed little during those events. Genetic analyses highlighted the low genetic connectivity and long‐term persistence of populations, and the founder effect and genetic drift seemed to have been very important processes that shaped the current diversity and genetic structure observed in both genomes. The genetic singularity of each population clearly shows the need for in situ conservation of all of them.     

The hidden history of the snowshoe hare,Lepus americanus: extensive mitochondrial DNA introgression inferred from multilocus genetic variation

Hybridization drives the evolutionary trajectory of many species or local populations, and assessing the geographic extent and genetic impact of interspecific gene flow may provide invaluable clues to understand population divergence or the adaptive relevance of admixture. In North America, hares (Lepus spp.) are key species for ecosystem dynamics and their evolutionary history may have been affected by hybridization. Here we reconstructed the speciation history of the three most widespread hares in North America – the snowshoe hare (Lepus americanus), the white‐tailed jackrabbit (L. townsendii) and the black‐tailed jackrabbit (L. californicus) – by analysing sequence variation at eight nuclear markers and one mitochondrial DNA (mtDNA) locus (6240 bp; 94 specimens). A multilocus–multispecies coalescent‐based phylogeny suggests that L. americanus diverged ~2.7 Ma and that L. californicus and L. townsendii split more recently (~1.2 Ma). Within L. americanus, a deep history of cryptic divergence (~2.0 Ma) was inferred, which coincides with major speciation events in other North American species. While the isolation‐with‐migration model suggested that nuclear gene flow was generally rare or absent among species or major genetic groups, coalescent simulations of mtDNA divergence revealed historical mtDNA introgression from L. californicus into the Pacific Northwest populations of L. americanus. This finding marks a history of past reticulation between these species, which may have affected other parts of the genome and influence the adaptive potential of hares during climate change.