Changes In Effective Population Size Research Articles

Population Genomic Scans for Natural Selection and Demography.

Uncovering the fundamental processes that shape genomic variation in natural populations is a primary objective of population genetics. These processes include demographic effects such as past changes in effective population size or gene flow between structured populations. Furthermore, genomic variation is affected by selection on nonneutral genetic variants, for example, through the adaptation of beneficial alleles or balancing selection that maintains genetic variation. In this article, we discuss the characterization of these processes using population genetic models, and we review methods developed on the basis of these models to unravel the underlying processes from modern population genomic data sets. We briefly discuss the conditions in which these approaches can be used to infer demography or identify specific nonneutral genetic variants and cases in which caution is warranted. Moreover, we summarize the challenges of jointly inferring demography and selective processes that affect neutral variation genome-wide.

Pitfalls and windfalls of detecting demographic declines using population genetics in long-lived species.

Detecting recent demographic changes is a crucial component of species conservation and management, as many natural populations face declines due to anthropogenic habitat alteration and climate change. Genetic methods allow researchers to detect changes in effective population size (Ne) from sampling at a single timepoint. However, in species with long lifespans, there is a lag between the start of a decline in a population and the resulting decrease in genetic diversity. This lag slows the rate at which diversity is lost, and therefore makes it difficult to detect recent declines using genetic data. However, the genomes of old individuals can provide a window into the past, and can be compared to those of younger individuals, a contrast that may help reveal recent demographic declines. To test whether comparing the genomes of young and old individuals can help infer recent demographic bottlenecks, we use forward-time, individual-based simulations with varying mean individual lifespans and extents of generational overlap. We find that age information can be used to aid in the detection of demographic declines when the decline has been severe. When average lifespan is long, comparing young and old individuals from a single timepoint has greater power to detect a recent (within the last 50 years) bottleneck event than comparing individuals sampled at different points in time. Our results demonstrate how longevity and generational overlap can be both a hindrance and a boon to detecting recent demographic declines from population genomic data.

Habitat quality or quantity? Niche marginality across 21 plants and animals suggests differential responses between highland and lowland species to past climatic changes

Climatic changes can affect species distributions, population abundance, and evolution. Such organismal responses could be determined by the amount and quality of available habitats, which can vary independently. In this study, we assessed changes in habitat quantity and quality independently to generate explicit predictions of the species' responses to climatic changes between Last Glacial Maximum (LGM) and present day. We built ecological niche models for genetic groups within 21 reptile, mammal, and plant taxa from the Baja California peninsula inhabiting lowland or highland environments. Significant niche divergence was detected for all clades within species, along with significant differences in the niche breadth and area of distribution between northern and southern clades. We quantified habitat quantity from the distribution models, and most clades showed a reduction in distribution area towards LGM. Further, niche marginality (used as a measure of habitat quality) was higher during LGM for most clades, except for northern highland species. Our results suggest that changes in habitat quantity and quality can affect organismal responses independently. This allows the prediction of genomic signatures associated with changes in effective population size and selection pressure that could be explicitly tested from our models.

Does coevolution in refugia drive mimicry in bumble bees? Insights from a South Asian mimicry group.

Müllerian mimicry was proposed to be an example of a coevolved mutualism promoted by population isolation in glacial refugia. This, however, has not been well supported in butterfly models. Here, we use genomic data to test this theory while examining the population genetics behind mimetic diversification in a pair of co-mimetic bumble bees, Bombus breviceps Smith and Bombus trifasciatus Smith. In both lineages, populations were structured by geography but not as much by color pattern, suggesting sharing of color alleles across regions of restricted gene flow and formation of mimicry complexes in the absence of genetic differentiation. Demographic analyses showed mismatches between historical effective population size changes and glacial cycles, and niche modeling revealed only mild habitat retraction during glaciation. Moreover, mimetic subpopulations of the same color form in the two lineages only in some cases exhibit similar population history and genetic divergence. Therefore, the current study supports a more complex history in this comimicry than a simple refugium-coevolution model.

Historical Demography and Climate Driven Range Shifts in the Blue-spotted Salamander Under the Climate Change Scenarios

This study integrates phylogeography with distributional analysis to understand the demographic history and range dynamics of a limited dispersal capacity amphibian species, Blue-spotted Salamander (Ambystoma laterale), under several climate change scenarios. For this we used an ecological niche modeling approach, together with Bayesian based demographic analysis, to develop inferences regarding this species' demographic history and range dynamics. The current model output was mostly congruent with the present distribution of the Blue-spotted Salamander. However, under both the Last Interglacial and the Last Glacial Maximum bioclimatic conditions, the model predicted a substantially narrower distribution than the present. These predictions showed almost no suitable area in the current distribution range of the species during almost the last 22.000 y before present (ybp). The predictions indicated that the distribution of this species shifted from eastern coast of northern North America to the southern part of the current distribution range of the species. The Bayesian Skyline Plot analysis, which provided good resolution of the effective population size changes over the Blue-spotted Salamander history, was mostly congruent with ecological niche modeling predictions for this species. This study provides the first investigation of the Blue-spotted Salamander’s late-Quaternary history based on ecological niche modeling and Bayesian-based demographic analysis. In terms of the main result of this study, we found that the species' present genetic structure has been substantially affected by past climate changes, and this species has reached current distribution range almost from nothing since the Last Glacial Maximum.

Changes in effective population size of Odonata in response to climate change revealed through genomics

The advent of third generation sequencing technologies has led to a boom of high-quality, chromosome level genome assemblies of Odonata, but to date, these have not been widely used to estimate the demographic history of the sequenced species through time. Yet, an understanding of how lineages have responded to past changes in the climate is useful in predicting their response to current and future changes in the climate. Here, we utilized the pairwise sequential markovian coalescent (PSMC) to estimate the demographic histories of Sympetrum striolatum, Ischnura elegans, and Hetaerina americana, three Odonata for which chromosome-length genome assemblies are available. Ischnura elegans showed a sharp decline in effective population size around the onset of the Pleistocene ice ages, while both S. striolatum and H. americana showed more recent declines. All three species have had relatively stable population sizes over the last one hundred thousand years. Although it is important to remain cautious when determining the conservation status of species, the coalescent models did not show any reason for major concern in any of the three species tested. The model for I. elegans confirmed prior research suggesting that population sizes of I. elegans will increase as temperatures rise.

Comparative genetic and demographic responses to climate change in three peatland butterflies in the Jura massif

Climate is a main driver of species distributions, but all species are not equally affected by climate change, and their differential responses to similar climatic constraints might dramatically affect the local species composition. In the context of climate warming, a better knowledge of the ability of dispersal-limited and habitat-specialist species to track climate change at local scale is urgently needed. Comparing the population genetic and demographic impacts of past climate cycles in multiple co-distributed species with similar ecological requirements help predicting the community-scale response to climate warming, but such comparative studies remain rare. Here, we studied the relationship between demographic history and past changes in spatial distribution of three protected peatland butterfly species (Boloria aquilonaris, Coenonympha tullia, Lycaena helle) in the Jura massif (France), using a genomic approach (ddRAD sequencing) and species distribution modeling (SDM). We found a similar and narrow thermal niche among species, and shared demographic histories of post-glacial decline and recent fragmentation of populations. Each species functions as a single metapopulation at the regional scale, with a North-South gradient of decreasing genetic diversity that fits the local dynamics of the ice cover over time. However, we found no correlation between changes in the quantity or the quality of suitable areas and changes in effective population size over time. This suggests that species ranges moved beyond the Jura massif during the less favorable climatic periods, and/or that habitat loss and deterioration are major drivers of the current dramatic decline observed in the three species. Our findings allow better understanding how history events and contemporary dynamics shape local biodiversity, providing valuable knowledge to identify appropriate conservation strategies.

De Novo Whole Genome Assemblies for Two Southern African Dwarf Chameleons (Bradypodion, Chamaeleonidae).

A complete and high-quality reference genome has become a fundamental tool for the study of functional, comparative, and evolutionary genomics. However, efforts to produce high-quality genomes for African taxa are lagging given the limited access to sufficient resources and technologies. The southern African dwarf chameleons (Bradypodion) are a relatively young lineage, with a large body of evidence demonstrating the highly adaptive capacity of these lizards. Bradypodion are known for their habitat specialization, with evidence of convergent phenotypes across the phylogeny. However, the underlying genetic architecture of these phenotypes remains unknown for Bradypodion, and without adequate genomic resources, many evolutionary questions cannot be answered. We present de novo assembled whole genomes for Bradypodion pumilum and Bradypodion ventrale, using Pacific Biosciences long-read sequencing data. BUSCO analysis revealed that 96.36% of single copy orthologs were present in the B. pumilum genome and 94% in B. ventrale. Moreover, these genomes boast scaffold N50 of 389.6 and 374.9 Mb, respectively. Based on a whole genome alignment of both Bradypodion genomes, B. pumilum is highly syntenic with B. ventrale. Furthermore, Bradypodion is also syntenic with Anolis lizards, despite the divergence between these lineages estimated to be nearly 170 Ma. Coalescent analysis of the genomic data also suggests that historical changes in effective population size for these species correspond to notable shifts in the southern African environment. These high-quality Bradypodion genome assemblies will support future research on the evolutionary history, diversification, and genetic underpinnings of adaptation in Bradypodion.

A comparison of genomic diversity and demographic history of the North Atlantic and Southwest Atlantic southern right whales.

Right whales (genus Eubalaena) were among the first, and most extensively pursued, targets of commercial whaling. However, understanding the impacts of this persecution requires knowledge of the demographic histories of these species prior to exploitation. We used deep whole genome sequencing (~40×) of 12 North Atlantic (E. glacialis) and 10 Southwest Atlantic southern (E. australis) right whales to quantify contemporary levels of genetic diversity and infer their demographic histories over time. Using coalescent- and identity-by-descent-based modelling to estimate ancestral effective population sizes from genomic data, we demonstrate that North Atlantic right whales have lived with smaller effective population sizes (Ne) than southern right whales in the Southwest Atlantic since their divergence and describe the decline in both populations around the time of whaling. North Atlantic right whales exhibit reduced genetic diversity and longer runs of homozygosity leading to higher inbreeding coefficients compared to the sampled population of southern right whales. This study represents the first comprehensive assessment of genome-wide diversity of right whales in the western Atlantic and underscores the benefits of high coverage, genome-wide datasets to help resolve long-standing questions about how historical changes in effective population size over different time scales shape contemporary diversity estimates. This knowledge is crucial to improve our understanding of the right whales' history and inform our approaches to address contemporary conservation issues. Understanding and quantifying the cumulative impact of long-term small Ne, low levels of diversity and recent inbreeding on North Atlantic right whale recovery will be important next steps.

Review of population history reconstruction methods in conservation biology

Demographic history reconstruction is based on the estimation of effective population size (Ne), which is inferred and interpreted in various fields of evolutionary and conservation biology. Interest in Ne estimation is growing, as the key evolutionary forces and their are linked to Ne, and genetic data become increasingly accessible. However, what is effective population size, and how can we obtain an estimate of effective population size? In this review, we describe the history of the term Ne and explore existing methods for obtaining historical and contemporary estimates of changes in effective population size. We provide a detailed overview of methods based on sequential Markovian coalescence (SMC), generalized phylogenetic coalescence (G-PhoCS), identity by descent (IBD) and identity by state (IBS) similarity, as well as methods using allele frequency spectrum (AFS). For each method, we briefly summarize the underlying theory and note its advantages and disadvantages. In the final section of the review, we present examples of the use of these methods for various non-model species with conservation status.

Population Genomics Provide Insights into the Evolution and Adaptation of the Asia Corn Borer.

Understanding the genetic basis of pest adaptive evolution and the risk of adaptation in response to climate change is essential for the development of sustainable agricultural practices. However, the genetic basis of climatic adaptation for the Asian corn borer (ACB), Ostrinia furnacalis, the main pest of corn in Asia and Oceania, is poorly understood. Here, we revealed the genomic loci underlying the climatic adaptation and evolution in ACB by integrating population genomic and environmental factors. We assembled a 471-Mb chromosome-scale reference genome of ACB and resequenced 423 individuals covering 27 representative geographic areas. We inferred that the ACB effective population size changes tracked with the global temperature and followed by a recent decline. Based on an integrated analysis of whole-genome selection scans and genome-wide genotype-environment association studies, we revealed the genetic basis of ACB adaption to diverse climates. For diapause traits, we identified a major effect association locus containing a circadian clock gene (period) by analyzing a diapause-segregating population. Moreover, our predictions indicated that the northern populations were more ecologically resilient to climate change than the southern populations. Together, our results revealed the genomic basis for ACB environmental adaptation and provided potential candidate genes for future evolutionary studies and genetic adaptation to climate change, intending to maintain the efficacy and sustainability of novel control techniques.

Species-specific traits mediate avian demographic responses under past climate change.

Anticipating species' responses to environmental change is a pressing mission in biodiversity conservation. Despite decades of research investigating how climate change may affect population sizes, historical context is lacking, and the traits that mediate demographic sensitivity to changing climate remain elusive. We use whole-genome sequence data to reconstruct the demographic histories of 263 bird species over the past million years and identify networks of interacting morphological and life history traits associated with changes in effective population size (Ne) in response to climate warming and cooling. Our results identify direct and indirect effects of key traits representing dispersal, reproduction and survival on long-term demographic responses to climate change, thereby highlighting traits most likely to influence population responses to ongoing climate warming.

Genetic and Ecological Divergence of Cinnamon Hummingbird Amazilia rutila (Aves: Trochilidae) Continental Populations Separated by Geographical and Environmental Barriers

Background and Research Aims: Historical geological events and climatic changes have played important roles in shaping population differentiation and distribution within species. Amazilia rutila (Trochilidae) is a widespread hummingbird species in the tropical dry forest along the Pacific slope and the Yucatán Peninsula in Mexico. Methods: We used mitochondrial DNA sequence, ecological niche modelling and niche divergence tests to determine the effects of major geographic barriers and environmental variability on genetic and niche divergence of A. rutila continental populations. Results: Our results revealed three genetic groups without haplotype sharing corresponding to the distribution of individuals/populations from the Pacific slope W of the Isthmus of Tehuantepec (PAC), in Oaxaca and Chiapas E of the Isthmus of Tehuantepec (CHIS_OAX) and those from the Yucatán Peninsula and Guatemala (YUC). Values of neutrality tests suggest past demographic expansion without effective population size changes over time, and the time since the demographic expansion ranged between 39.4 and 84.45 ka BP. Each genetic group differed in their position in environmental space, with low-to-very limited overlap in the fundamental climatic niche dimensions of all groups analyzed, particularly between YUC and PAC. Analysis of climate differentiation and ecological niche comparisons showed that the environmental space occupied by these mtDNA groups is similar but not identical. Conclusion: We conclude that the genetic differentiation of A. rutila is consistent with a model of population isolation by geographical barriers and environmental differences. Inferences about the consequences of past demographic expansion and isolation underlying intraspecific evolutionary relationships await further study. Implications for Conservation: Our findings highlight the importance of preserving evolutionary significant units of this widespread hummingbird species. Conservation actions must consider intrinsic requirements of evolutionarily distinct populations and the environmental drivers that shape their distributions, maximizing preservation of intraspecific genetic variability and monitoring changes in genetic diversity.

Long‐term population decline of a genetically homogeneous continental‐wide top Arctic predator

Genetic analysis can provide valuable information for conservation programmes by unravelling the demographic trajectory of populations, estimating effective population size or inferring genetic differentiation between populations. Here, we investigated the genetic differentiation within Snowy Owls Bubo scandiacus in North America, a species identified as vulnerable by the IUCN, to (1) quantify connectivity among wintering areas, (2) evaluate current genetic diversity and effective population size, and (3) infer changes in the historical effective population size changes from the last millennia to the recent past. The Snowy Owl, a highly mobile top predator, breeds across the Arctic tundra, a region especially sensitive to current climate change. Using single‐nucleotide polymorphism (SNP)‐based analyses on Snowy Owls sampled across the North American non‐breeding range, we found an absence of genetic differentiation among individuals located up to 4650 km apart. Our results suggest high genetic intermixing and effective dispersal at the continental scale despite documented philopatry to non‐breeding sites in winter. Reconstructing the population demographic indicated that North American Snowy Owls have been steadily declining since the Last Glacial Maximum c. 20 000 years ago, and concurrently with global increases in temperature. Conservation programmes should now consider North American Snowy Owls a single, genetically homogeneous continental‐wide population which is probably sensitive to the long‐term global warming occurring since the Last Glacial Maximum.

Whole genome demographic models indicate divergent effective population size histories shape contemporary genetic diversity gradients in a montane bumble bee.

Understanding historical range shifts and population size variation provides an important context for interpreting contemporary genetic diversity. Methods to predict changes in species distributions and model changes in effective population size (N e) using whole genomes make it feasible to examine how temporal dynamics influence diversity across populations. We investigate N e variation and climate-associated range shifts to examine the origins of a previously observed latitudinal heterozygosity gradient in the bumble bee Bombus vancouverensis Cresson (Hymenoptera: Apidae: Bombus Latreille) in western North America. We analyze whole genomes from a latitude-elevation cline using sequentially Markovian coalescent models of N e through time to test whether relatively low diversity in southern high-elevation populations is a result of long-term differences in N e. We use Maxent models of the species range over the last 130,000 years to evaluate range shifts and stability. N e fluctuates with climate across populations, but more genetically diverse northern populations have maintained greater N e over the late Pleistocene and experienced larger expansions with climatically favorable time periods. Northern populations also experienced larger bottlenecks during the last glacial period, which matched the loss of range area near these sites; however, bottlenecks were not sufficient to erode diversity maintained during periods of large N e. A genome sampled from an island population indicated a severe postglacial bottleneck, indicating that large recent postglacial declines are detectable if they have occurred. Genetic diversity was not related to niche stability or glacial-period bottleneck size. Instead, spatial expansions and increased connectivity during favorable climates likely maintain diversity in the north while restriction to high elevations maintains relatively low diversity despite greater stability in southern regions. Results suggest genetic diversity gradients reflect long-term differences in N e dynamics and also emphasize the unique effects of isolation on insular habitats for bumble bees. Patterns are discussed in the context of conservation under climate change.

Changes in human effective population size overlap the beginning and end of a critical time in European medieval history, also characterized by the Black Death epidemic

The intersection of historiography and archaeology has long pondered over the impact of known historical events on census size. In recent times, genetic methods have successfully traced changes over time in the genetic size of a given population. Moreover, the correlation between genetic and census sizes of a population is contingent on several demographic assumptions that are relatively simple for our species. Our research endeavours to examine the changes in effective population size (Ne) in all human populations in the 1000 Genomes Project over the past two millennia. We compared our findings with estimates from historical censuses where available. Our investigation confirms what was already observed in France and reveals a common pattern found in most European populations, which manifests as a drastic population decrease beginning around the year 1300 and growth after the year 1600. This profile aligns well with known wars, famines, and epidemics that characterized these trying times in Europe. The most notable among them being the second plague epidemic, caused by Y. pestis, which in Europe commenced in 1347/8 and is also known as the "Black Death". Our findings demonstrate that changes in genetic population size through time can serve as a dependable proxy for census size, which is independent of potential biases in the written historical record. Consequently, we provide a robust estimate of the impact caused by the population crisis that followed the year 1300 on the European genomic landscape in light of previous results. Our study offers a new paradigm for interpreting the past and underscores the potential of genetic methods in reconstructing historical events.

Migration pulsedness alters patterns of allele fixation and local adaptation in a mainland-island model.

Geneflow across populations is a critical determinant of population genetic structure, divergence, and local adaptation. While evolutionary theory typically envisions geneflow as a continuous connection among populations, many processes make it fluctuating and intermittent. We analyze a mainland-island model where migration occurs as recurrent "pulses." We derive mathematical predictions regarding how the level of migration pulsedness affects the effective migration rate, for neutral and selected mainland alleles. We find that migration pulsedness can either decrease or increase geneflow, depending on the selection regime. Pulsedness increases geneflow for sufficiently (counter)selected alleles (s<s1), but reduces it otherwise. We provide a mathematical approximation of the threshold selection strength s1, which is verified in stochastic simulations. Migration pulsedness thus affects the fixation rate at different loci in opposite directions, in a way that cannot be described as a change in effective population size. We show that migration pulsedness would generally reduce the level of local adaptation and introduce an additional genetic load: the "pulsedness load." This is detrimental to the adaptation and persistence of small peripheral populations, with implications in management and conservation. These results indicate temporal variability in migration patterns may be an important, yet understudied, controller of geneflow and local adaptation.

Minor Genetic Consequences of a Major Mass Mortality: Short-Term Effects in Pisaster ochraceus.

AbstractMass mortality events are increasing globally in frequency and magnitude, largely as a result of human-induced change. The effects of these mass mortality events, in both the long and short term, are of imminent concern because of their ecosystem impacts. Genomic data can be used to reveal some of the population-level changes associated with mass mortality events. Here, we use reduced-representation sequencing to identify potential short-term genetic impacts of a mass mortality event associated with a sea star wasting outbreak. We tested for changes in the population for genetic differentiation, diversity, and effective population size between pre-sea star wasting and post-sea star wasting populations of Pisaster ochraceus-a species that suffered high sea star wasting-associated mortality (75%-100% at 80% of sites). We detected no significant population-based genetic differentiation over the spatial scale sampled; however, the post-sea star wasting population tended toward more differentiation across sites than the pre-sea star wasting population. Genetic estimates of effective population size did not detectably change, consistent with theoretical expectations; however, rare alleles were lost. While we were unable to detect significant population-based genetic differentiation or changes in effective population size over this short time period, the genetic burden of this mass mortality event may be borne by future generations, unless widespread recruitment mitigates the population decline. Prior results from P. ochraceus indicated that natural selection played a role in altering allele frequencies following this mass mortality event. In addition to the role of selection found in a previous study on the genomic impacts of sea star wasting on P. ochraceus, our current study highlights the potential role the stochastic loss of many individuals plays in altering how genetic variation is structured across the landscape. Future genetic monitoring is needed to determine long-term genetic impacts in this long-lived species. Given the increased frequency of mass mortality events, it is important to implement demographic and genetic monitoring strategies that capture baselines and background dynamics to better contextualize species' responses to large perturbations.

Paracoccidioides restrepiensis has undergone a severe population bottleneck

Genus Paracoccidioides now encompasses five species, P. lutzii, P. brasiliensis sensu stricto, P. americana, P. venezuelensis, and P. restrepiensis. All the paracoccidioidomycosis (PCM) cases reported in Colombia have been classified as P. restrepiensis, which was named in honor of Angela Restrepo, a leading researcher in the field of the biology of the fungus. Previous assessments of genetic diversity have suggested that Paracoccidioides species have differences in their level of polymorphism. To infer changes in effective population size, we used the Pairwise sequentially Markovian coalescent (PSMC) by generating two pseudodiploids for P. restrepiensis and one for P. brasiliensis sensu stricto. We found that P. restrepiensis diverged from its sister species recently, the divergence time from P. venezuelensis being 125,000 (± 42,000) years. The analyses using PSMC show a systematic reduction in the effective population size of P. restrepiensis with a rapid decrease in genetic variability compared to P. brasiliensis sensu stricto, which indicates that P. restrepiensis has undergone a systematic population bottleneck. None of the other two species show the dramatic effective population size reduction observed in P. restrepiensis. These comparisons suggest that the trajectory of P. restrepiensis is somehow different from the other Paracoccidioides species and poses the question regarding the biogeographic events that have led to such a dramatic population pattern.

Different Interspecies Demographic Histories within the Same Locality: A Case Study of Sea Cucumbers, Cuttlefish and Clams in Greek Waters

Coalescent methods in population genetics aim to detect biodiversity patterns, evolutionary mechanisms, and signatures of historical changes in effective population sizes with respect to the species fidelity. Restriction site-associated DNA sequencing (RADseq) was used to evaluate the population dynamics of invertebrate species within the same localities. New sequencing technologies, such as the ones employed by population genetics, could be used to improve the management and sustainability of marine and aquaculture resources. Sea cucumbers (Holothuria tubolosa) showed genetic differentiation patterns favoring limited gene flow between studied areas. Similar results for clams (Venus verrucosa) suggest local adaptation and low-dispersal abilities for sessile organisms. On the contrary, cuttlefish (Sepia officinalis) exhibited a panmictic pattern, resulting in a single genetic stock in the area. The larvae settlement duration may be responsible for such interspecies variations. Interspecies demographic modeling revealed different environmental pressures of historical events’ signatures with respect to the three invertebrates. Sea cucumbers favor a post-glacial bottleneck event followed by a more recent recovery, whereas cuttlefish favor an expansion before the late glacial maximum. Lastly, clams showed a constant effective population size in the area. The results of historical demographic changes in natural populations provide opportunities for critical evaluation and management in terms of the conservation of the species in the area.