Spatially explicit models of dynamic histories: examination of the genetic consequences of Pleistocene glaciation and recent climate change on the American Pika

A central goal of phylogeography is to identify and characterize the processes underlying divergence. One of the biggest impediments currently faced is how to capture the spatiotemporal dynamic under which a species evolved. Here, we described an approach that couples species distribution models (SDMs), demographic and genetic models in a spatiotemporally explicit manner. Analyses of American Pika (Ochotona princeps) from the sky islands of the central Rocky Mountains of North America are used to provide insights into key questions about integrative approaches in landscape genetics, population genetics and phylogeography. This includes (i) general issues surrounding the conversion of time-specific SDMs into simple continuous, dynamic landscapes from past to current, (ii) the utility of SDMs to inform demographic models with deme-specific carrying capacities and migration potentials as well as (iii) the contribution of the temporal dynamic of colonization history in shaping genetic patterns of contemporary populations. Our results support that the inclusion of a spatiotemporal dynamic is an important factor when studying the impact of distributional shifts on patterns of genetic data. Our results also demonstrate the utility of SDMs to generate species-specific predictions about patterns of genetic variation that account for varying degrees of habitat specialization and life history characteristics of taxa. Nevertheless, the results highlight some key issues when converting SDMs for use in demographic models. Because the transformations have direct effects on the genetic consequence of population expansion by prescribing how habitat heterogeneity and spatiotemporal variation is related to the species-specific demographic model, it is important to consider alternative transformations when studying the genetic consequences of distributional shifts.     

Demographic inference from whole‐genome and RAD sequencing data suggests alternating human impacts on goose populations since the last ice age

We investigated how population changes and fluctuations in the pink‐footed goose might have been affected by climatic and anthropogenic factors. First, genomic data confirmed the existence of two separate populations: western (Iceland) and eastern (Svalbard/Denmark). Second, demographic inference suggests that the species survived the last glacial period as a single ancestral population with a low population size (100–1,000 individuals) that split into the current populations at the end of the last glacial maximum with Iceland being the most plausible glacial refuge. While population changes during the last glaciation were clearly environmental, we hypothesize that more recent demographic changes are human‐related: (1) the inferred population increase in the Neolithic is due to deforestation to establish new lands for agriculture, increasing available habitat for pink‐footed geese, (2) the decline inferred during the Middle Ages is due to human persecution, and (3) improved protection explains the increasing demographic trends during the 20th century. Our results suggest both environmental (during glacial cycles) and anthropogenic effects (more recent) can be a threat to species survival.     

Historical demography of freshwater mussels (Bivalvia: Unionidae): genetic evidence for population expansion and contraction during the late Pleistocene and Holocene

Genetic variation was examined in two endangered mussel species, Epioblasma brevidens and Epioblasma capsaeformis, and in a non‐listed species, Lampsilis fasciola, in the Clinch River, Tennessee, USA, by screening mitochondrial DNA (mtDNA) sequences and nuclear DNA microsatellites. Patterns of mtDNA polymorphism exhibited different trends in long‐term population sizes for each species during the late Pleistocene and Holocene (～20 000 ya to present); namely, E. brevidens has declined over time, E. capsaeformis has remained demographically stable, and L. fasciola has expanded. However, analyses using microsatellites did not exhibit similar trends, perhaps because homoplasy had eliminated long‐term population signatures for the loci examined. For both marker types, long‐term effective population size (N_e) was low in E. brevidens, intermediate in E. capsaeformis, and high in L. fasciola. Moderately diverged mtDNA lineages, perhaps indicative of secondary contact, were observed in E. brevidens and E. capsaeformis. Perhaps the most surprising result of this study was the high level of genetic variation observed at both mtDNA and microsatellite DNA markers for L. fasciola, variation seemingly contrary to the relatively small demes that currently reside in the Clinch River. However, the data are consistent with known demographic and life‐history traits of these three mussel species and their fish hosts, namely that they each use hosts with different dispersal capabilities, ranging from low, moderate, and high, respectively. The low divergence of mtDNA sequence variation reported in this and other recent mussel studies indicates that considerable extant population genetic variation probably originated during the late Pleistocene and Holocene. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 376–397.     

Combining phylogeography and landscape genetics of Xenopipo atronitens (Aves: Pipridae), a white sand campina specialist,to understand Pleistocene landscape evolution in Amazonia

Open vegetation (campinas and campinaranas) associated with white sand patches occurs in the form of islands in a forested matrix throughout the Amazon basin. Bird species restricted to these habitats have patchy distributions, although connectivity may have been influenced by past glacial cycles as a result of the substitution of forest by savanna. Because these landscape changes are a matter of debate in the history of Amazonia, we studied the diversification of Xenopipo atronitens, a white sand specialist, aiming to infer the effects of past climate changes. The split of Xenopipo atronitens from its sister species, Xenopipo uniformis, may be related to Tepuis erosion and retreat of escarpments during the Miocene, or to a dispersal event. Compared with birds from terra firme forest, X. atronitens has low genetic structure. Low levels of unidirectional gene flow were found from the Guyana Shield to adjacent areas. Demographic expansion starting approximately 25 kyr BP was detected for some populations and is probably related to the Last Glacial Maximum and subsequent climate improvement. Landscape genetic analyses indicate that the forested (terra firme) matrix acts as a barrier for the dispersal of X. atronitens. The results of the present study indicate that glacial cycles have deeply influenced Amazonian biogeographical history, demonstrating a complex interaction between forest and nonforest habitats during the Pleistocene. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 60–76.     

Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines

Historical information suggests the occurrence of an extensive human-caused contraction in the distribution range of wolves (Canis lupus) during the last few centuries in Europe. Wolves disappeared from the Alps in the 1920s, and thereafter continued to decline in peninsular Italy until the 1970s, when approximately 100 individuals survived, isolated in the central Apennines. In this study we performed a coalescent analysis of multilocus DNA markers to infer patterns and timing of historical population changes in wolves surviving in the Apennines. This population showed a unique mitochondrial DNA control-region haplotype, the absence of private alleles and lower heterozygosity at microsatellite loci, as compared to other wolf populations. Multivariate, clustering and Bayesian assignment procedures consistently assigned all the wolf genotypes sampled in Italy to a single group, supporting their genetic distinction. Bottleneck tests showed evidences of population decline in the Italian wolves, but not in other populations. Results of a Bayesian coalescent model indicate that wolves in Italy underwent a 100- to 1000-fold population contraction over the past 2000-10,000 years. The population decline was stronger and longer in peninsular Italy than elsewhere in Europe, suggesting that wolves have apparently been genetically isolated for thousands of generations south of the Alps. Ice caps covering the Alps at the Last Glacial Maximum (c. 18,000 years before present), and the wide expansion of the Po River, which cut the alluvial plains throughout the Holocene, might have provided effective geographical barriers to wolf dispersal. More recently, the admixture of Alpine and Apennine wolf populations could have been prevented by deforestation, which was already widespread in the fifteenth century in northern Italy. This study suggests that, despite the high potential rates of dispersal and gene flow, local wolf populations may not have mixed for long periods of time.     

Rise and fall of a wolf population: genetic diversity and structure during recovery,rapid expansion and drastic decline

The grey wolves (Canis lupus) of Finland have had a varied history, with a period of rapid population expansion after the mid‐1990s followed by a decline with a current census size of about 140 wolves. Here, we investigate the impact of unstable population size and connectivity on genetic diversity and structure in a long‐term genetic study of 298 Finnish wolves born in 1995–2009 and genotyped for 17 microsatellite loci. During the initial recovery and prior to population expansion, genetic diversity was high (1995–1997: LD‐N_e = 67.2; H_o = 0.749; H_e = 0.709) despite a small census size and low number of breeders (N_c < 100; N_b < 10) likely reflecting the status of the Russian source population. Surprisingly, observed heterozygosity decreased significantly during the study period (t = ?2.643, P = 0.021) despite population expansion, likely a result of an increase in inbreeding (F_IS = 0.108 in 2007–2009) owing to a low degree of connectivity with adjacent Russian wolf population (m = 0.016–0.090; F_ST = 0.086, P < 0.001) and population crash after 2006. However, population growth had a temporary positive impact on N_e and number of family lines. This study shows that even strong population growth alone might not be adequate to retain genetic diversity, especially when accompanied with low amount of subsequent gene flow and population decline.     

Genetic variation,population structure and cryptic species within the black mudfish,Neochanna diversus,an endemic galaxiid from New Zealand

To investigate the phylogenetic relationships and geographical structure among landlocked populations of the black mudfish, Neochanna diversus, mitochondrial DNA nucleotide sequence data were sampled from seven populations from the Waikato and Northland regions of New Zealand. The complete D-loop region was sequenced from 70 individuals, with 913 bp from the tRNA-pro end used in population and phylogenetic analysis. A tandem repeat array, which ranged in size up to 200 bp, was found in most populations at the 3′ end of the D-loop that was not able to be aligned for analysis. Of the seven sites sampled, two from Northland exhibited significant sequence divergence from all other sites. There was also a clear distinction among remaining Northland sites and those from the Waikato. An additional 518 bp segment of the 16S region was sequenced from all sites and compared with the other New Zealand mudfish species, N. apoda, N. burrowsius and the Tasmanian mudfish Galaxias (Neochanna) cleaveri using Galaxias maculatus as an outgroup. Both D-loop and 16S sequence data provided strong evidence for a cryptic species of mudfish present in Northland. The significant genetic structure apparent in the black mudfish appears most probably to be attributed to geological conditions during the Pliocene, where peat wetlands became apparent in the Waikato while Northland consisted of disjunct ‘islands’. Conservation and management of these populations must take into account the historical processes that have shaped these patterns of genetic diversity.     

Survival,density and population composition of bellbirds (Anthornis melanura) on the Poor Knights Islands,New Zealand

Abstract

Annual survival by age, sex and population size and structure were estimated for bellbirds (Anthornis melanura) from a banding study undertaken on 66 ha Aorangi Island, the Poor Knights Islands, during the period 1978–86. The most parsimonious model showed that survival varied little with age and between years, and survival of males was significantly greater than that of females. Recapture probabilities of males and females were similar, but did vary with age and among years. There was a greater proportion of adult males than adult females and sub‐adult males and females in the population, and among adults the male bias in the population was greater during the breeding season than at other times of the year. The high density of bellbirds on the Poor Knights and larger size of males may explain the reduced survival of females relative to that of males.     

Sailing through the Late Pleistocene: unusual historical demography of an East Asian endemic, the Chinese Hwamei (Leucodioptron canorum canorum), during the last glacial period

Pleistocene climate fluctuations shaped the patterns of genetic diversity observed in extant species. In contrast to Europe and North America where the effects of recent glacial cycles on genetic diversity have been well studied, the genetic legacy of the Late Pleistocene for East Asia, a region of great topographical complexity and presumably milder historical climate, remains poorly understood. We analysed 3.86 kb of the mitochondrial genome of 186 Chinese Hwamei birds, Leucodioptron canorum canorum , and found that contrary to the conventional expectation of population decline during cold periods (stadials), the demographic history of this species shows continuous population growth since the penultimate glacial period (about 170 000 years ago). Refugia were identified in the south, coastal regions, and northern inland areas, implying that topographic complexity played a substantial role in providing suitable habitats for the Chinese Hwamei during cold periods. Intermittent gene flow between these refugia during the warmer periods (interstadials) might have resulted in a large effective population of this bird through the last glacial period.     

Effective number of white shark (Carcharodon carcharias,Linnaeus) breeders is stable over four successive years in the population adjacent to eastern Australia and New Zealand

Population size is a central parameter for conservation; however, monitoring abundance is often problematic for threatened marine species. Despite substantial investment in research, many marine species remain data‐poor presenting barriers to the evaluation of conservation management outcomes and the modeling of future solutions. Such is the case for the white shark (Carcharodon carcharias), a highly mobile apex predator for whom recent and substantial population declines have been recorded in many globally distributed populations. Here, we estimate the effective number of breeders that successfully contribute offspring in one reproductive cycle (Nb) to provide a snapshot of recent reproductive effort in an east Australian–New Zealand population of white shark. Nb was estimated over four consecutive age cohorts (2010, 2011, 2012, and 2013) using two genetic estimators (linkage disequilibrium; LD and sibship assignment; SA) based on genetic data derived from two types of genetic markers (single nucleotide polymorphisms; SNPs and microsatellite loci). While estimates of Nb using different marker types produced comparable estimates, microsatellite loci were the least precise. The LD and SA estimates of Nb within cohorts using SNPs were comparable; for example, the 2013 age cohort Nb(SA) was 289 (95% CI 200–461) and Nb(LD) was 208.5 (95% CI 116.4–712.7). We show that over the time period studied, Nb was stable and ranged between 206.1 (SD ± 45.9) and 252.0 (SD ± 46.7) per year using a combined estimate of Nb(LD+SA) from SNP loci. In addition, a simulation approach showed that in this population the effective population size (Ne) per generation can be expected to be larger than Nb per reproductive cycle. This study demonstrates how breeding population size can be monitored over time to provide insight into the effectiveness of recovery and conservation measures for the white shark, where the methods described here may be applicable to other data‐poor species of conservation concern.     

Range expansion during the Pleistocene drove morphological radiation of the fir genus (Abies,Pinaceae) in the Qinghai‐Tibet Plateau and Himalayas

Range expansion caused by climate oscillations in the past probably promoted morphological radiation in a few plant groups. In this study, we aim to test this hypothesis through phylogeographical analysis of the cold‐tolerant fir genus (Abies) in the Qinghai‐Tibet Plateau (QTP) and Himalayas, where it comprises 12 described species. We examined sequence variation in two maternally inherited mitochondrial (mt) DNA fragments (nad5‐4 and nad7‐1) and two paternally inherited plastid DNA fragments (trnS‐G and trnL‐F) for 733 individuals from 75 populations of the species in a monophyletic group. Only six mtDNA haplotypes were recovered, but five were shared between multiple species and one occurred at a high frequency, providing strong evidence of range expansion. Forty‐three plastid DNA haplotypes were detected, 19 of which were shared between species and three occurred at high frequency. Network, mismatch and Bayesian skyline plot analyses of all plastid DNA haplotypes from this clade clearly suggested range expansion. This expansion was dated as having occurred during the longest and most extensive glaciation in the Pleistocene. Our results therefore supported the range expansion hypothesis for this clade of Abies during the Pleistocene; expansion probably drove the morphological radiation of the clade in the QTP and Himalayas, although it remains unclear whether the different morphotypes should be acknowledged as independent, reproductively isolated species. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 444–453.     

Phylogeography of the Alpine salamander, Salamandra atra (Salamandridae) and the influence of the Pleistocene climatic oscillations on population divergence

Fifty individuals of the endemic Alpine salamander, Salamandra atra, representing 13 populations throughout the range of the two currently recognized subspecies, atra and aurorae, were examined for sequence variation in a large portion (1050 bp) of the mitochondrial cytochrome b gene. We revealed a large number of mitochondrial DNA (mtDNA) haplotypes (10). Interpopulation sequence divergence was very low, ranging from 0 to 3.1%. The relationships among haplotypes were poorly resolved. The divergence time estimate between several mtDNA haplotypes suggested a pre-Pleistocene differentiation approximately 3 million years ago. Moreover, the impact of the Pleistocene glaciations on the phylogeographical patterns appears to have been secondary, although a somewhat reduced genetic variability was found in populations living in areas that were directly affected by the glaciation.     

Genetic diversity, population structure, and conservation of Sophora moorcroftiana (Fabaceae), a shrub endemic to the Tibetan Plateau

Sophora moorcroftiana is a perennial leguminous low shrub endemic to the middle reaches of Yarlung Zangbo River in Tibet. It is an important species to fix sand dunes and to avoid the formation of shifting sands; therefore, its progressive over-exploitation may enhance land desertification. The levels and distribution of genetic variability of this species were evaluated from 10 natural populations at 24 loci encoding 13 enzymes, using allozyme analysis by starch gel electrophoresis. Data obtained revealed moderate levels of genetic variation within populations (Pp=27.5%, Ap=1.5, Hep=0.122) and a considerable divergence among populations (FST=0.199). Significant positive correlations (r2=0.49, p<0.05; r2=0.46, p<0.05) were found between elevation and both mean number of alleles per locus (A) and gene diversity (He) in the studied populations of S. moorcroftiana. Lower genetic diversity in lower elevation populations might be due to the negative effects of human pressures and habitat fragmentation, to adaptation to high altitudes as a consequence of a peripatric speciation process, or to directional gene flow along the river basin from the source populations located in the west at higher altitudes. The evaluation of the degree of threat has led to the inclusion of this species in the category of EN ("endangered"), and conservation strategies for this endemic species are discussed on the basis of these findings.     

Reproduction and growth of the black shore skink,Leiolopisma suteri (Lacertilia: Scincidae), in north‐eastern New Zealand

Reproduction and growth of a boulder beach population of the nocturnal skink Leiolopisma suteri on Motutapu Island were studied for 19 months. Epididymes contain sperm from April to November, and copulation probably occurs in October or November (spring). Ovulation occurs in late October or early November, and three or four (mean, 3.7) eggs are laid in late December. Incubation takes 3 months. Total development time from ovulation to hatching is 5 months, one of the longest development periods recorded for Scincidae. Growth to sexual maturity is slow, most females depositing their first clutch 33 months after hatching; males mature at 29 months.     

Species status and population genetic structure of the flightless chafer beetles Prodontria modesta and P. bicolorata (Coleoptera; Scarabaeidae) from South Island, New Zealand

This study uses isozyme electrophoresis to investigate the systematic status of two rare flightless chafer beetle species, Prodontria modesta and P. bicolorata , currently distinguished solely on the basis of colour. Seven polymorphic loci were analysed for the species in sympatry and allopatry. In sympatry, gene frequencies imply no genetic barrier between the two colour forms. Wright's hierarchical F-statistics were calculated to determine how the genetic variation is partitioned across the geographic range of the two species. Strong geographic structuring occurs at the population level but there is little genetic differentiation attributable to species. Comparisons of morphological measurements are in support of the electrophoretic results. The systematic significance of the two distinct colour forms is thus questionable. Under the biological, recognition or phylogenetic species concepts, the genetic data suggest that there is only one species, polytypic for a colour pattern. Most of the genetic diversity of this group of beetles lies within and among populations, which differ quite markedly over their geographic range, rather than between the two named species.     

Depth Distribution and Abundance of the Common Bully, Gobiomorphus cotidianus (Eleotridae), in Three Oligotrophic New Zealand Lakes, One of which is Turbid

The depth distribution of the common bully, Gobiomorphus cotidianus, a small benthic forage fish, was measured by trapping at set depths from 0–70m in three large oligotrophic lakes, including one where inorganic sediment from a glacially-fed river produces turbid conditions. Bullies occurred at all depths from 0.5–70m in the clear lakes, but none were present below 25m in the turbid lake. Two groups of bullies were present in the clear lakes; a high-density, littoral stock at depths of 0.5–25m, and a low-density, profundal stock at depths of 30–70m. These groups were further distinguished by differing buoyancy requirements and feeding habits. The swimbladders of littoral bullies contained gas, but those of the profundal bullies, which fed more than littoral bullies by both day and night, did not. The variation in mean CPUE with depth within the littoral zone was not related to water temperature, oxygen concentration, or conductivity. Nor was it related to a reduction in light levels or to reduced water transparency caused by increased turbidity. It may therefore be controlled by biotic factors. The absence of a profundal stock below the littoral zone in the turbid lake indicates that the settlement of fines from turbid inputs may affect bully abundance in deeper waters. As conventional measures of the abundance of benthic fish in lakes are often restricted to littoral habitats, and do not reflect changes in abundance with depth, an index of overall abundance based on depth distribution was developed to allow comparisons between lakes.     

Isolation and characterization of microsatellite loci from Lochmaea suturalis, the heather beetle (Coleoptera: Chrysomelidae), a pest in Europe and a biocontrol agent in New Zealand

The heather beetle Lochmaea suturalis which is native to northwest Europe has been released as a biocontrol agent for heather in New Zealand. We have isolated and optimized eight microsatellite loci from New Zealand beetles. These loci provide markers with high polymorphism ranging from four to 20 alleles per locus. Observed heterozygosity averaged 0.631 per locus. These results suggest the markers are useful for population studies that will contribute to assessment of L. suturalis as a biocontrol agent.     

Home‐ranges,population densities,vocal behavior,and post‐fledging movements of Cipo Canasteros (Asthenes luizae,Furnariidae), a rock‐specialist endemic of the highlands of eastern Brazil

Cipo Canasteros (Asthenes luizae, Furnariidae) have a fragmented and limited range restricted to the campos rupestres (rupestrian grasslands) habitat in the Brazilian highlands of the Espinhaço Range, and little is known about their behavior, ecology, and population biology. From March 2009 to November 2010, we monitored birds (24 banded and 22 radio‐tracked) at two study sites at Serra do Cipó in the state of Minas Gerais, Brazil, to estimate their home‐range sizes and population density, and describe their habitat use, natal dispersal behavior, and vocal behavior. We found an average density of 8.7 paired adults/km² in our study areas or 22.9 paired adults/km² when considering only used habitats. The sex ratio was male‐biased (males/total adults = 0.68), adults exhibited high site fidelity, home‐ranges averaged 4.0 ha (fixed kernel 95%) or 3.5 ha (95% minimum convex polygon) in size, and both sexes defended territories year‐round. We recorded four main types of songs, including two uttered more often during the breeding season. We monitored the natal dispersal of two males and one female who moved maximum distances of 1238 m, 780 m, and 1056 m, respectively, from natal areas. Our results confirm that Cipo Canasteros are restricted to the rocky‐outcrop habitat of the campos rupestres. In part due to their habitat specialization, Cipo Canasteros are considered Near Threatened, but other factors contributing to their demographic fragility include the small number, and probably low survival, of females and low reproductive success due to predation and brood parasitism by cowbirds. Given these threats, along with their specialized habitat and restricted range, the future conservation of Cipo Canasteros will likely depend on the extent to which their campos rupestres habitat can be conserved.     

Response of nannoplankton to major changes in sea-surface temperature and movements of hydrological fronts over Site DSDP 594 (south Chatham Rise, southeastern New Zealand), during the last 130 kyr

A high-resolution history of paleoceanographic changes in the subpolar waters of the southern margin of the Subtropical Convergence Zone during the last 130 kyr, is present in foraminiferal assemblages of DSDP Site 594. The foraminifera indicate that sea-surface temperatures during the Last Interglacial Climax were warmer than today, and that between substage 5d through to the end of isotope stage 2, temperatures were mostly cooler than Holocene temperatures. The paleotemperatures suggest that (1) the Subtropical Convergence was located over the site during substage 5e, later moving further north, then moving southwards to near the site during the Holocene, and (2) the Polar Front was positioned over the Site during glacial stages 6, 4, 2 and possibly parts of stage 3. Several major events are indicated by the nannofloral assemblages during these large changes in sea-surface temperature and associated reorganization of ocean circulation. First, the time-progressive trends between E. huxleyi and medium to large Gephyrocapsa are unique to this site, with E. huxleyi dominating over medium Gephyrocapsa during stages 5c-a, middle part of stage 4 and after the middle point of stage 3. This unusual trend may (at least partly) be caused by the shift of the Polar Front across the site. Second, upwelling flora (E. huxleyi and small placoliths) increase in abundance during stages 1, 3 and 5, suggesting that upwelling or disturbance of water stratification took place during the interglacials. Thirdly, there are no significant differences between the distribution patterns of the various morphotypes of medium to large Gephyrocapsa, and the combined value of all medium Gephyrocapsa increases in abundance during glacials (stages 2 and 4 and the end of stage 6), similar to the abundance trends in benthic foraminifera. Finally, subordinate nannofossil taxa also show distinctive. climatic trends during the last glacial cycle: (1) Syracosphaera spp. are present in increased abundance during warmer extremes in climate (substages 5e, 5a, and stage 1); (2) Coccolithus pelagicus and Calcidiscus leptoporus dominate the subordinate nannofossil taxa, and their relative proportions seem to provide a useful paleoceanographic index, with C. pelagicus dominating when the Polar Front Zone is over the site (stages 6, 4 and 2), whilst C. leptoporus is relatively more abundant when the STC is positioned over the site (stages 1 and 5e). Increased abundance of C. pelagicus also can indicate intensified coastal upwelling.