Integrating Population Genetics Research Articles

Environmental suitability throughout the late quaternary explains population genetic diversity

Genetic variation among populations is reflected in biogeographic patterns for many species, but general rules of spatial genetic variation have not been established. In this paper, we establish a theoretical framework based on projecting environmental Grinellian niches back through time to relate the present geographic distribution of population genetic structure to a given species' historical evolutionary context. Thanks to advances in next‐generation sequencing technologies, as well as more accurate climate models and the amassing of information stored in biological collections, it is possible to implement this theoretical framework directly. We develop a case study of the tassel‐eared squirrel Sciurus aberti to jointly analyze spatial, environmental, and genetic data to predict the historical endemic area of this species. Our results reveal that in cases of genetic isolation by geographic distance, the prevalence of environmental suitability over time corresponds to the genetic fixation index (Fst) of populations with respect to a source population. Populations closer to the historical endemic area show higher genetic diversity and a lower Fst value. This empirical example relates back to the theoretical framework, allowing two further advances: 1) a layer of biogeographic explanation for the results obtained from population genomic methods; and 2) predictive maps of this genetic structure to support biodiversity conservation efforts. Overall, this work advances a perspective that integrates population genetics with historical patterns of species distribution. The limitations posed in the theoretical framework should be considered before implementing the suitability prevalence area (SPA) in a general way over different taxa. Otherwise, the predictability of the genetic diversity of populations as a product of environmental stability over time may not be adequate.

Integrating Population Genetics With Long-Term Environmental Monitoring to Evaluate and Guide Vernal Pool Creation for Amphibian Conservation.

The decline of biodiversity, particularly among amphibians, is strongly associated with habitat loss and fragmentation. Vernal pools are a critical ecosystem for many pool-breeding amphibians, but they are often overlooked in wetland protection guidelines. Mitigation efforts include vernal pool creation and restoration, but these efforts have varying success in replacing lost functions. This study investigates the success of created vernal pools through long-term environmental monitoring of wood frogs and spotted salamanders (2014-2023) and integrates population genetics to assess the local population health of the wood frog. First, we monitored and compared environmental parameters and reproductive success of indicator species between natural and created pools in a Pennsylvania state park. We then used microsatellite loci to assess within- and between-pool measures of genetic diversity, population structuring, and gene flow for wood frogs. We found two carefully designed created pools positively contributed to local amphibian population persistence by maintaining similar measures of genetic diversity as compared to natural pools. On the other hand, one poorly created pool was genetically distinct and acted as a population sink. Although our findings offer valuable insights, they are based on a limited sample and may not fully represent the broader landscape. However, by integrating genetic information into long-term monitoring datasets, our interdisciplinary approach enhances our understanding of amphibian population dynamics in vernal pool ecosystems. Our findings imply that the most important factors for restoration practitioners to consider when creating or restoring vernal pools are hydroperiod (12-35 weeks), volume (> 50 m3), depth (≥ 30 cm), and surrounding forest land cover (> 60%). These variables are better predictors of indicator species success than pool type (i.e., natural or created). Ultimately, this study emphasizes the need to accompany restoration efforts with long-term monitoring programs that can be used to make adaptive management decisions in an era of extreme environmental change.

Integrating population genetics, stem cell biology and cellular genomics to study complex human diseases.

Human pluripotent stem (hPS) cells can, in theory, be differentiated into any cell type, making them a powerful in vitro model for human biology. Recent technological advances have facilitated large-scale hPS cell studies that allow investigation of the genetic regulation of molecular phenotypes and their contribution to high-order phenotypes such as human disease. Integrating hPS cells with single-cell sequencing makes identifying context-dependent genetic effects during cell development or upon experimental manipulation possible. Here we discuss how the intersection of stem cell biology, population genetics and cellular genomics can help resolve the functional consequences of human genetic variation. We examine the critical challenges of integrating these fields and approaches to scaling them cost-effectively and practically. We highlight two areas of human biology that can particularly benefit from population-scale hPS cell studies, elucidating mechanisms underlying complex disease risk loci and evaluating relationships between common genetic variation and pharmacotherapeutic phenotypes.

Integrating population genetics and species distribution modelling to guide conservation of the noble crayfish, Astacus astacus, in Croatia

The noble crayfish, Astacus astacus, is an indigenous European freshwater species. Its populations show significant declines caused by anthropogenic pressure on its habitats, climate change and the spread of invasive species. Diminishing populations’ trends and loss of genetic diversity highlight the need for effective conservation that will ensure their long-term survival. We combined population genetics and species distribution modelling (SDM) to reveal the impact of climate change and invasive species on the noble crayfish, and to guide future conservation programs of current populations. Our study showed that Croatian populations of A. astacus harbour an important part of species genetic diversity and represent significant genetic reservoir at the European level. The SDM results predicted substantial reductions of suitable habitats for A. astacus by the 2070; only 13% of its current potential distribution is projected to remain stable under pessimistic Representative Concentration Pathway (RCP 8.5) emission scenario. Moreover, most of the populations with high genetic diversity are located in the areas predicted to become unsuitable, and consequently have a high probability of being lost in the future. Further, SDM results also indicated considerable decrease of future habitat suitability for invasive crayfish species in Croatia, suggesting that climate change poses a major threat to already endangered A. astacus. The obtained results help in the identification of populations and areas with the highest conservation value which should be given the highest priority for protection. In order to preserve present diversity in areas that are predicted as suitable, we propose assisted migration and repopulation approaches, for enhancing populations’ size and saving maximum genetic variability. The result of our research emphasizes once again the benefits of multidisciplinary approach in the modern biodiversity conservation.

Inferring the impact of past climate changes and hunting on the South American sea lion

AbstractAimMany pinniped species have experienced drastic demographic changes due to their interaction with humans. Most studies, however, have failed to detect recent bottlenecks in otariids from genetic data. The South American Sea Lion Otaria flavescens have a long history of population changes associated with interglacial expansion and hunting to almost extinction. This study aimed at investigating these different demographic fluctuations integrating population genetics and phylogeographic approaches.LocationPacific coast of South America.MethodsEighty‐five samples from the Chilean coast were collected. Eight microsatellite loci were genotyped, and D‐Loop mitochondrial DNA (mtDNA) sequenced. Genetic diversity was assessed, and tests of recent genetic bottlenecks were performed. Past demographic changes were inferred based on neutrality tests, adjustment of a sudden expansion model and Bayesian skyline plots. The magnitude and timing of the different population size changes were further investigated through approximate Bayesian computation (ABC) of coalescent inferences.ResultsThe mtDNA shows relatively high diversity (h = 0.98 and π = 0.01) compared to most otariids, corroborates the divergence between Pacific and Atlantic populations, around 80,000 years ago (ya), and revealed a secondary contact zone in the Magellan strait. Microsatellite data support a second genetic discontinuity at 40°S, associated with post‐glacial colonization of Patagonia. ABC analyses confirmed that glaciation affected the effective population size (Ne) all along the Pacific Coast, between ~50,000 and 15,000 ya. A strong reduction of Ne was also inferred for the hunting period (73–66 ya from sampling).Main conclusionsO. flavescens shows clear signatures of susceptibility to climatic and anthropogenic disturbances and a spatial genetic structure that should be taken into account in the context of management and conservation policies. Yet, despite a recent history of demographic bottlenecks, the genetic diversity remains high, likely a consequence of the demographic dynamics in otariids, characterized by large and connected metapopulations.

Demo-Genetic Approach for the Conservation and Restoration of a Habitat-Forming Octocoral: The Case of Red Coral, Corallium rubrum, in the Réserve Naturelle de Scandola

Marine protected areas (MPAs) are one of the most efficient conservation tools to buffer marine biodiversity loss induced by human activities. Beside effective enforcement, an accurate understanding of the eco-evolutionary processes underlying the patterns of biodiversity is needed to reap the benefits of management policies. In this context, integrating population genetics with demographic data, the demo-genetic approach, is particularly relevant to shift from a “species-based pattern” toward an “eco-evolutionary-based processes” conservation. Here, targeting a key species in the Mediterranean coralligenous, the red coral, Corallium rubrum, in an emblematic Mediterranean MPA, the “Réserve Naturelle de Scandola” (France), we applied demo-genetic approaches at two contrasted spatial scales, among populations and within one population, to (i) infer the demographic connectivity among populations in the metapopulation network and (ii) shed new light on the genetic connectivity and on the demographic transitions underlying the dynamics of a near-pristine population. Integrating different spatial and temporal scales, we demonstrated (i) an apparent temporal stability in the pattern of genetic diversity and structure in the MPA in spite of a dramatic demographic decline and (ii) contrasted levels of genetic isolation but substantial demographic connectivity among populations. Focusing on the near-pristine population, we complemented the characterization of red coral demographic connectivity suggesting (iii) temporal variability and (iv) the occurrence of collective dispersal. In addition, we demonstrated (v) contrasted patterns of spatial genetic structure (SGS), depending on the considered stage-class (adults vs. juveniles), in the near-pristine population. This last result points out that the overall SGS resulted from a restricted dispersal of locally produced juveniles (SGS among adults and juveniles) combined to mortality during early life stages (decrease of SGS from juveniles to adults). Demonstrating the occurrence of two management units and the importance of two populations (CAVB and ALE) for the network of connectivity, we made recommendations for the management of the Réserve Naturelle de Scandola. Besides, we contributed to the implementation of scientifically driven restoration protocols in red coral by providing estimates for the size, density, and distances among patches of transplanted colonies.

Primate landscape genetics: A review and practical guide.

Landscape genetics is an emerging field that integrates population genetics, landscape ecology, and spatial statistics to investigate how geographical and environmental features and evolutionary processes such as gene flow, genetic drift, and selection structure genetic variation at both the population and individual levels, with implications for ecology, evolution, and conservation biology. Despite being particularly well suited for primatologists, this method is currently underutilized. Here, we synthesize the current state of research on landscape genetics in primates. We begin by outlining how landscape genetics has been used to disentangle the drivers of diversity, followed by a review of how landscape genetic methods have been applied to primates. This is followed by a section highlighting special considerations when applying the methods to primates, and a practical guide to facilitate further landscape genetics studies using both existing and de novo datasets. We conclude by exploring future avenues of inquiry that could be facilitated by recent developments as well as underdeveloped applications of landscape genetics to primates.

Genotyping on the ark: A synthesis of genetic resources available for species in zoos.

Using molecular genetic information to guide population management can improve the sustainability of species in captivity. However, empirical population genetics has not been commonly applied to species management programs in zoos. One limitation may be the availability of genetic resources (e.g., markers, primers, etc.) for species held in zoos. To assess the extent to which species held in zoos have been studied using population genetics in the wild, we conducted a systematic literature review of close to 8,000 papers. We synthesized information on the availability and scale of population genetics studies across amphibian, bird, mammal, and reptile species held in zoos, and discussed their potential for informing ex situ management. We found that more than half of the species in zoos (52%) already have some genetic markers described in the literature specific for them, or a congeneric species, that could be further developed to aid the management of zoo populations, and the accumulation of these resources has been steady over the past decades. Furthermore, the proportion of species with genetic resources is even higher (62%) for species that are being managed through a formal breeding program in zoos. Our study provides encouraging results for captive program managers interested in integrating population genetics into ex situ management strategies.

Back to the future of a rare plant species of the Chihuahuan desert: tracing distribution patterns across time and genetic diversity as a basis for conservation actions

Habitat fragmentation and its effects on the persistence of populations and species are of major concern to conservation biology. Penstemon coriaceus is a rare and endemic species from the Mexican Central Plateau and adjacent foothills of the Sierra Madre Occidental and Sierra Madre Oriental, which belongs to the Chihuahuan Desert ecoregion. This is the first study that integrates population genetics and ecological niche modeling analysis as tools to understand the distribution and genetic diversity patterns of a Penstemon species. We used AFLP markers for 144 individuals across 11 populations, and calibrated Ecological niche modeling for three different time periods (current, future and past). Population genetics analysis showed low levels of genetic diversity at the population level and high genetic differentiation among populations. Ecological niche modeling analysis revealed an important decline of the distribution range due to climate change, which can be considered as an indicator for the vulnerability of temperate forest. The integration of both methods revealed that the genetic differentiation observed only show a relationship with the environment variables and the habitat suitability, but not with the geographical distribution of the populations sampled; which indicate the importance of the environmental factors in the determination of genetic processes for P. coriaceus.

Integrating population genetics in an adaptive management framework to inform management strategies

Adequate levels of genetic diversity are important for long term persistence of wildlife species, yet genetic principles have only been considered in the last few years when developing management plans for conservation purposes. We present here an example on how genetic management plans can be explicitly integrated into an adaptive management framework. This can be achieved by developing a predictive model to explore population responses to different management options, and by quantifying management targets that should be verified through monitoring programs. We apply this approach to the woylie or brush tailed bettong (Bettongia penicillata); an Australian macropod, listed as Critically Endangered. Results suggest that discrete small populations (e.g. 30 woylies/year over the course of several years is recommended. Formal completion of the adaptive management approach would include, in addition to the stages presented here, a quantitative assessment of the outcome of management and continue refinement of the modelling framework on the basis of new data gained through ongoing monitoring. We encourage the formal inclusion of genetic management within the adaptive management framework as demonstrated in this study.

Integrating population genetics to define conservation units from the core to the edge of Rhinolophus ferrumequinum western range.

The greater horseshoe bat (Rhinolophus ferrumequinum) is among the most widespread bat species in Europe but it has experienced severe declines, especially in Northern Europe. This species is listed Near Threatened in the European IUCN Red List of Threatened Animals, and it is considered to be highly sensitive to human activities and particularly to habitat fragmentation. Therefore, understanding the population boundaries and demographic history of populations of this species is of primary importance to assess relevant conservation strategies. In this study, we used 17 microsatellite markers to assess the genetic diversity, the genetic structure, and the demographic history of R. ferrumequinum colonies in the western part of its distribution. We identified one large population showing high levels of genetic diversity and large population size. Lower estimates were found in England and northern France. Analyses of clustering and isolation by distance suggested that the Channel and the Mediterranean seas could impede R. ferrumequinum gene flow. These results provide important information to improve the delineation of R. ferrumequinum management units. We suggest that a large management unit corresponding to the population ranging from Spanish Basque Country to northern France must be considered. Particular attention should be given to mating territories as they seem to play a key role in maintaining high levels of genetic mixing between colonies. Smaller management units corresponding to English and northern France colonies must also be implemented. These insular or peripheral colonies could be at higher risk of extinction in the near future.

Landscape Genetics of Mammals in American Ecosystems

Since the term was coined in 2003, landscape genetics (LG) is a field that integrates population genetics, landscape ecology, and spatial analytical techniques to quantify the effects of landscape on microevolutionary processes. Despite the growing interest in LG, there is little knowledge about the trends in LG research for America in general and regarding mammals in particular, as well as about which ecosystems are being most studied. Deserts represent nearly one-third of the Earth’s surface and are characterized by high heterogeneity and species richness. However, they are underrepresented in the LG literature. Hence, we performed a thorough review of published scientific articles addressing LG of mammals in America, with emphasis on deserts. The objectives were to 1) determine the mammal groups that have been most studied; 2) establish the representation of desert ecosystems; 3) describe the research questions and analytical methods most frequently used; and 4) summarize the key landscape factors and environmental variables associated with genetic diversity and structure patterns of mammals in America. We conducted a comprehensive literature search of published articles between 2003 and 2019 in the Web of Science (http://apps.webofknowledge.com) based on search words specific to the revision subject. We verified and screened the articles recovered, and gathered basic information (species, authors, publication year), together with the research questions addressed and the genetic and statistical methods used. We recovered 36 publications on LG involving mammals in America; of these, only eight were conducted on desert ecosystems (Table 1). Rodentia was the most represented order in all American ecosystems (n = 20), while Artiodactyla (n = 4) was specifically represented in deserts. Of all studies, the most common research questions focused on estimating ‘connectivity’ (n = 14) and ‘genetic structure’ (n = 12), and the most frequent analytical methods were Mantel and partial Mantel tests. Dispersal capabilities and vegetation cover were the most important variables regarding the genetic structure of desert populations. Most studies evaluated connectivity with simple and partial Mantel tests, but the use of novel methodologies (i. e., genomics) was also identified. Ecological traits of species, particularly for rodents, and vegetation cover were the main factors related to genetic patterns in deserts. Notably, we identified that North America is the most studied region, while LG studies with mammals are scarce in Mexico and South America (one study encompassed North and Central America), as well as in desert ecosystems, hence the urgency to conduct studies in those regions and in deserts.

On the proportional abundance of species: Integrating population genetics and community ecology

The frequency of genes in interconnected populations and of species in interconnected communities are affected by similar processes, such as birth, death and immigration. The equilibrium distribution of gene frequencies in structured populations is known since the 1930s, under Wright’s metapopulation model known as the island model. The equivalent distribution for the species frequency (i.e. the species proportional abundance distribution (SPAD)), at the metacommunity level, however, is unknown. In this contribution, we develop a stochastic model to analytically account for this distribution (SPAD). We show that the same as for genes SPAD follows a beta distribution, which provides a good description of empirical data and applies across a continuum of scales. This stochastic model, based upon a diffusion approximation, provides an alternative to neutral models for the species abundance distribution (SAD), which focus on number of individuals instead of proportions, and demonstrate that the relative frequency of genes in local populations and of species within communities follow the same probability law. We hope our contribution will help stimulate the mathematical and conceptual integration of theories in genetics and ecology.

Accounting for uncertainty in predictions of a marine species: Integrating population genetics to verify past distributions

We develop a new perspective on the uncertainties affecting the predictions of coastal species distributions using patterns of genetic diversity to assess the congruence of hindcasted distribution models. We model the niche of the subtidal seagrass Cymodocea nodosa, for which previous phylogeographic findings are used to contrast hypotheses for the Last Glacial Maximum (LGM) in the Mediterranean and adjacent Atlantic coastal regions. We focus on amelioration of sampling bias, and explore the influence of other sources of uncertainty such as the number of variables, Ocean General Circulation Models (OGCMs), and thresholds used. To do that, we test geographical and environmental filtering of presences, and a species-specific weighted filter related to political boundaries for background data. Contrary to our initial hypothesis that reducing sampling bias by means of geographical, environmental or background filtering would enhance predictive power and reliability of the models, none of these approaches consistently improved performance. These counter-intuitive results might be explained by the higher relative occurrence area (ROA) inherent to linear coastal study areas in relation to terrestrial regions, which may cause worse predictions and, thus, higher variability among models. We found that the Ocean General Circulation Models (OGCMs), the threshold and, to a smaller extent, the number of variables used, conditioned greatly the variability of the predictions in both accuracy and geographic range. Despite these uncertainties, all models achieved the goal of identifying long-term persistence regions (glacial refugia) where the highest genetic diversity for Cymodocea nodosa is found nowadays. However, only the CCSM corroborated the hypothesis, raised in previous studies, of a vicariant process in shaping the species’ genetic structure.

Regional adaptation defines sensitivity to future ocean acidification

Physiological responses to temperature are known to be a major determinant of species distributions and can dictate the sensitivity of populations to global warming. In contrast, little is known about how other major global change drivers, such as ocean acidification (OA), will shape species distributions in the future. Here, by integrating population genetics with experimental data for growth and mineralization, physiology and metabolomics, we demonstrate that the sensitivity of populations of the gastropod Littorina littorea to future OA is shaped by regional adaptation. Individuals from populations towards the edges of the natural latitudinal range in the Northeast Atlantic exhibit greater shell dissolution and the inability to upregulate their metabolism when exposed to low pH, thus appearing most sensitive to low seawater pH. Our results suggest that future levels of OA could mediate temperature-driven shifts in species distributions, thereby influencing future biogeography and the functioning of marine ecosystems.

Contrasting patterns of population connectivity between regions in a commercially important mollusc Haliotis rubra: integrating population genetics, genomics and marine LiDAR data

Estimating contemporary genetic structure and population connectivity in marine species is challenging, often compromised by genetic markers that lack adequate sensitivity, and unstructured sampling regimes. We show how these limitations can be overcome via the integration of modern genotyping methods and sampling designs guided by LiDAR and SONAR data sets. Here we explore patterns of gene flow and local genetic structure in a commercially harvested abalone species (Haliotis rubra) from southeastern Australia, where the viability of fishing stocks is believed to be dictated by recruitment from local sources. Using a panel of microsatellite and genomewide SNP markers, we compare allele frequencies across a replicated hierarchical sampling area guided by bathymetric LiDAR imagery. Results indicate high levels of gene flow and no significant genetic structure within or between benthic reef habitats across 1400km of coastline. These findings differ to those reported for other regions of the fishery indicating that larval supply is likely to be spatially variable, with implications for management and long-term recovery from stock depletion. The study highlights the utility of suitably designed genetic markers and spatially informed sampling strategies for gaining insights into recruitment patterns in benthic marine species, assisting in conservation planning and sustainable management of fisheries.

Genetic Diversity of the Endemic Xantus’ Hummingbird Using 16 Novel Polymorphic Microsatellite Loci, and Their Cross Amplification between Six Related Species

A set of 16 microsatellite loci was developed and characterized for the Xantus’ hummingbird (Hylocharis xantusii) by using 454 next-generation sequencing. Twenty-five H. xantusii samples from one population were genotyped; all loci were polymorphic, with the number of alleles ranging from three to ten. The mean observed heterozygosity was 0.681 for all loci. No significant linkage disequilibrium was detected, but five loci (Hxan05, 06, 09, 13 and 14) showed deviation from Hardy-Weinberg equilibrium. These microsatellite loci are the first to be characterized for H. xantusii. A moderate to high level of cross-species amplification was observed across the six hummingbird species (31% - 87.5%), with the best cross amplification results observed in the closest related species (H. leucotis, Cynanthus latirostris, Calypte costae). The availability of these molecular tools allows assessing questions integrating population genetics, ecology, conservation, and evolutionary history for H. xantusii and for other phyogenetically related species.

Integrating Analyses of Population Genetics and Space-Time Information for Wildlife Management: An Empirical Study on Japanese Wild Boar Populations

This study is a “model study” of how to apply the findings of molecular ecological studies to wildlife management, aimed at showing the importance of analyses integrating population genetics, space-time information and bioinformatics methods. We chose the Japanese wild boar (Sus scrofa leucomystax) in Tochigi Prefecture, Japan, because its captured area has been spreading in recent years. We used 72 adult individuals gathered by hunters in 2010. Three putative sub-populations were estimated using microsatellite DNA. Our study indicated that the individuals newly found in the northern area originated from other prefectures, not from different areas within the same prefecture, and no inobuta (crossbreeding with pigs) in the maternal line were found. Comparing the number of mutations obtained by a coalescent simulation with that obtained by mitochondrial DNA, suggested that an assumed native population in the eastern area of Tochigi Prefecture was actually not native. Habitat preferences of the putative sub-populations, estimated by a generalized linear model, were different from each other, which also suggested that the boar could adjust its habitat based on the characteristics of the local environment. Risk maps, estimated using MaxEnt, based on past questionnaire surveys and those based on microsatellite DNA were different from each other.

Integrating population genetics and conservation biology in the era of genomics

As one of the final activities of the ESF-CONGEN Networking programme, a conference entitled 'Integrating Population Genetics and Conservation Biology' was held at Trondheim, Norway, from 23 to 26 May 2009. Conference speakers and poster presenters gave a display of the state-of-the-art developments in the field of conservation genetics. Over the five-year running period of the successful ESF-CONGEN Networking programme, much progress has been made in theoretical approaches, basic research on inbreeding depression and other genetic processes associated with habitat fragmentation and conservation issues, and with applying principles of conservation genetics in the conservation of many species. Future perspectives were also discussed in the conference, and it was concluded that conservation genetics is evolving into conservation genomics, while at the same time basic and applied research on threatened species and populations from a population genetic point of view continues to be emphasized.

Integrating population genetics and conservation biology: merging theoretical, experimental and applied approaches (Potsdam, Germany)

Integrating population genetics and conservation biology: merging theoretical, experimental and applied approaches (Potsdam, Germany)