Ongoing Gene Flow Research Articles

The genetic consequences of historic climate change on the contemporary population structure of a widespread temperate North American songbird

Studies of widely distributed species can inform our understanding of how past demographic events tied to historic glaciation and ongoing population genetic processes interact to shape contemporaneous patterns of biodiversity at a continental scale. In this study, we used whole-genome resequencing to investigate the current population structure and genetic signatures of past demographic events in the widespread migratory American goldfinch (Spinus tristis). Phylogenetic relationships inferred from whole mitochondrial genomes were poorly resolved. In contrast, a genome-wide panel of > 4.5 million single nucleotide polymorphisms (SNPs) strongly supported the existence of eastern and western populations separated by western mountain ranges and additional population structuring within the western clade. Demographic modeling estimated that the eastern and western populations diverged approximately one million years ago, and both populations experienced subsequent population bottlenecks during the last glacial period. Species distribution models showed a severe contraction of suitable habitat for the American goldfinch during this period, with predicted discontinuities that are consistent with multiple, isolated glacial refugia that coincide with present-day population structure. Low overall genetic differentiation between the eastern and western populations (FST ∼ 0.01) suggests ongoing gene flow accompanied divergence, and individuals with admixed genomic signatures were sampled along a potential contact zone. Nevertheless, outlier SNPs were identified near genes associated with feather color, song, and migratory behavior and provide strong candidates for further study of the mechanisms underlying reproductive isolation and speciation in birds.

Population genomic structure of the sea urchin Diadema africanum, a relevant species in the rocky reef systems across the Macaronesian archipelagos

The sea urchin Diadema africanum is a macro-herbivore found in the rocky reef systems of the West African region and Macaronesian archipelagos. Over several decades, high densities of this species have generated marine barrens in certain areas at the Canary Islands. In contrast, more recently, during the last few years, the species has suffered mass mortality events that continue to the present day. In this study, we used 9,109 Single Nucleotide Polymorphisms (SNPs) and a fragment of a mitochondrial gene to evaluate the species’ population structure, effects of mass mortalities on its diversity, and potential local adaptation across the Canary Islands and Cabo Verde. Our research provides compelling evidence of low genomic diversity and homogeneity across the studied area for neutral markers, along with recent demographic fluctuations. The high connectivity among distant areas likely allows a rapid recovering of the populations from local mortality events. Interestingly, we also observed genomic sub-structure from 405 SNPs identified as candidate loci under selection for seawater temperature. The lack of divergence among distant sites and the low diversity found can be attributed to the species’ divergence from a small ancestral genomic pool, followed by a contemporary demographic expansion, and ongoinggene flow.

Hybridization and introgression in deeply differentiated salamander species – molecular genetics and a reappraisal of Dr. Louis Vallée’s osteological data

Abstract Two morphologically and genetically distinct salamander species (the crested newt, Triturus cristatus and the marbled newt, T. marmoratus) engage over a large area in the west of France where they hybridize at ca. 4%. The species interaction is characterized by ecological differentiation and limited gene flow beyond the F1 hybrid generation. Incompletely isolated species like these allow to investigate the genetic mechanisms and evolutionary forces that maintain their identity in the face of ongoing gene flow, to which a large mosaic hybrid zone provides excellent opportunities. A reanalysis of published morphological data supports the partial breakdown of the species barrier whereas extensive genetic data show that introgression is low yet asymmetric, in line with the dynamics of species replacement inferred earlier. The current work, with seven diagnostic nuclear markers studied for a large sample, revises the estimates of introgression in both T. cristatus (to 0.24%) and T. marmoratus (to 0.11%). Difficulties remain in the recognition of potential triploid hybrids versus backcross hybrids. Haldane’s rule is partially supported, but deeper analyses require the use of a molecular marker for sex that is not yet available.

Measuring local genetic variation in permethrin-resistant head lice (Phthiraptera: Pediculidae) from Buenos Aires, Argentina.

The cosmopolitan ectoparasite human head louse, Pediculus humanus capitis (De Geer)(Phthiraptera:Pediculidae), affects mostly school-aged children, with infestations reported every year mainly due to louse resistance to pyrethroids. One of the main resistance mechanisms of pyrethroids is the target site insensitivity (kdr), which is caused by single-nucleotide point mutations (SNPs) located in the voltage-sensitive sodium channel gene. In this study, we analyzed individual head lice toxicologically via the description of their susceptibility profile to permethrin and genetically through the genotypification of their kdr alleles as well as nuclear microsatellite loci. Lice were collected from 4 schools in the city of Buenos Aires, Argentina. The resistance ratios varied from 33.3% to 71.4%, with a frequency of the T917I kdr mutation of 87.31% and with 83.6% of the head lice being homozygous resistant to pyrethroids. Microsatellite data indicated that all the louse school populations had genotype proportions that deviated from Hardy-Weinberg expectations, with FIS > 0 reflecting a deficit of heterozygotes. Bottleneck analysis suggested that all louse school populations underwent a recent reduction in population sizes, while 3 of the 4 schools had gene flow values around 1, indicating ongoing gene flow among those schools. Our study suggests that school louse populations in the city of Buenos Aires may form a metapopulation, where each school represents a small population that undergoes extinction and recolonization processes under strong permethrin selection. This is the first multilevel analysis integrating toxicological, kdr-genotyping, and microsatellite data in human louse populations.

Pleistocene climate oscillations have shaped the expansion and contraction speciation model of the globose Eriosyce sect. Neoporteria cacti in Central Chile.

Pleistocene climatic oscillations, characterized by arid (interglacial) and pluvial (glacial) phases, have profoundly impacted the floras of Mediterranean climates. Our study investigates the hypothesis that these climatic extremes have promoted phases of range expansion and contraction in the Eriosyce sect. Neoporteria, resulting in pronounced genetic structuring and restricted gene flow. Utilizing nuclear microsatellite markers, we genotyped 251 individuals across 18 populations, encompassing all 14 species and one subspecies within the Eriosyce sect. Neoporteria. Additionally, Species Distribution Models (SDMs) were employed to reconstruct past (Last Interglacial, Last Glacial Maximum, Mid-Holocene) and current potential distribution patterns, aiming to delineate the climatic influences on species' range dynamics. The gene flow analysis disclosed disparate levels of genetic interchange among species, with marked restrictions observed between entities that are geographically or ecologically separated. Notably, E. subgibbosa from Hualpen emerged as genetically distinct, warranting its exclusion for clearer genetic clustering into north, central, and south clusters. The SDMs corroborated these findings, showing marked range expansions during warmer periods and contractions during colder times, indicating significant shifts in distribution patterns in response to climatic changes. Our findings emphasize the critical role of Pleistocene climatic fluctuations in driving the dynamic patterns of range expansions and contractions that have led to geographic isolation and speciation within the Eriosyce sect. Neoporteria. Even in the face of ongoing gene flow, these climate-driven processes have played a pivotal role in sculpting the species' genetic architecture and diversity. This study elucidates the complex interplay between climatic variability and evolutionary dynamics among Mediterranean cacti in central Chile, highlighting the necessity of considering historical climatic millenial oscillations in conservation and evolutionary biology studies.

Environmentally associated colour divergence does not coincide with population structure across Lesser Antillean anoles

Abstract Species distributed across heterogeneous environments may undergo local adaptation, which can be limited by the homogenizing effects of gene flow. Lesser Antillean anoles exhibit dorsal colour variation associated with dramatic shifts in environment across small spatial scales, providing an excellent system for studying the maintenance of local adaptation despite ongoing gene flow. The 1995 Soufriere Hills eruption on Montserrat provides an opportunity to understand how natural disasters may influence the evolution of insular species. Thus, our study had two main objectives. First, we collected genetic, phenotypic, and environmental data to investigate whether environmentally associated dorsal coloration reflects underlying population structure in three species of Lesser Antillean anoles. Second, we examined the short-term evolutionary consequences of volcanism by comparing pre- and posteruption samples of Anolis lividus using multilocus sequence data. We found all three species exhibited genetic isolation-by-distance but not isolation-by-environment. Furthermore, phenotypic differences within each species were not predicted by genetic distances, suggesting gene flow across colour morphs. We confirmed the repopulation of A. lividus in the impacted area and found genetic diversity equivalent to pre-eruption sampling. Our findings contribute to our understanding of local adaptation in spatially small-scale systems and the impact of catastrophic natural disasters on population structure.

Intra-lake origin and rapid expansion of invasive pelagic three-spined stickleback in Lake Constance

The rapid expansion of three-spined stickleback (Gasterosteus aculeatus Linnaeus, 1758 (Perciformes, Gasterosteida)) in the pelagic zone of Lake Constance, Central Europe, since 2012 contributed to stark ecosystem-wide effects, such as food-web shifts and declines in native biodiversity, including commercially important fish species. Yet, the origin of this invasive pelagic population remains unclear. Using RAD-sequencing of Lake Constance sticklebacks, we show that the pelagic Lake Constance population likely arose recently within the lake, potentially from the littoral population. We did not detect any substantial genome-wide genetic differentiation between individuals from different habitats, supporting a recent origin of the pelagic population and/or ongoing gene flow. This is further supported by minimal differences in meristic and morphometric traits. However, we also identified multiple outlier loci between littoral and pelagic individuals across the genome, potentially suggesting early signs of adaptation despite high connectivity. In this study, we provide an important example of rapid within-lake ecological diversification of an invasive species from standing genetic variation. Ultimately, our findings will have major implications for the management of invasive pelagic stickleback, as they indicate that the stickleback population has to be managed as a whole and that management efforts cannot only focus on the hyper-abundant pelagic population.

Hybrid speciation driven by multilocus introgression of ecological traits

Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species1,2. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation3. Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus, which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.

DNA barcoding, phylogeography and evolutionary dynamics of Chrysichthys auratus

This study embarked on an exploration into the genetic structure and evolutionary history of the Chrysichthys auratus species, leveraging PCR amplification, phylogenetic trees, and haplotype networks. Specific DNA segments were successfully amplified and visualized through electrophoresis. Newly obtained sequences were Bank into GenBank and given accession numbers (OR730807-OR730808-OR730809). The Neighbor-Joining method provided insights into the evolutionary relationships among taxa, further augmented by bootstrap values and the Tamura 3-parameter method. A comprehensive geographical haplotype network showcased pronounced genetic differentiation, especially between remote populations. Nonetheless, shared haplotypes between proximate regions indicated either ancestral genetic connections or ongoing gene flow. Employing the COI-DNA barcodes, an in-depth understanding of intra- and inter-populational genetic diversity was achieved. The study's findings unravel the intricate genetic landscape and evolutionary dynamics of C. auratus, offering novel perspectives into its demographic history across its vast native habitat.

A shift in the host web occupancy of dew‐drop spiders associated with genetic divergence in the Southwest Pacific

AbstractAimWe assessed the population genetic structure of the kleptoparasitic spider Argyrodes bonadea across the Southwestern Pacific islands. Our aim is to evaluate the impact of overseas distances and, in particular, the Kerama gap, as potential drivers of genetic differentiation. If no relationship exists, then we assume dispersal following adaptive change as alternative non‐vicariant mechanism that generates divergence.LocationSouthwestern Pacific Islands.Taxon Argyrodes bonadea. MethodsWe used mitochondrial Cytochrome Oxidase 1 (CO1) gene sequences and Restriction Site‐associated DNA Sequencing (RAD‐seq) for our analyses.ResultsTwo strongly supported lineages, an Amami‐Okinawa Lineage (AOL) and an Austral‐Asia Lineage (AAL), correspond to two separate clades, roughly divided by the Kerama Gap, in phylogenetic trees estimated here. However, species delimitation led to the interpretation of only a single species present. The AOL exhibits complex, geographically structured host web spider species specificity, wherein the Amami population utilizes Cyrtophora, but AOL samples in Okinawa associate exclusively with Nephila—and yet all broadly distributed AAL populations show no evidence of host web spider species specificity.Main ConclusionThe population boundary between AOL and AAL likely results from local adaptation to novel hosts—instead of isolation by the Kerama Gap—following long‐distance dispersal and range expansion. Our results suggest kleptoparasitic spiders have the capacity to overcome permanent deep‐sea barriers and colonize distant landmasses. Whereas peripheral populations (AOL) demonstrate the capacity for specialization to a single host, which may have contributed to genetic differentiation and isolation, the broadly distributed AAL persists and has successfully expanded its geographical range as a host generalist, which may contribute to ongoing gene flow inferred in this study.

RADseq data reveal widespread historical introgression in four familiar North American songbirds.

Population genetic structure is influenced by a combination of contemporary and historical events; however, this structure can be complicated by ongoing gene flow. While it is well known that contemporary hybridization occurs frequently among many closely related species, it often remains uncertain as to which populations are involved in introgression events, and this can be even more difficult to infer when introgression is historical. Here we use restriction-site associated DNA sequencing to look at the level of introgression among four species of songbirds in North America: the black-capped, mountain, boreal, and chestnut-backed chickadee. Samples from both sympatric and allopatric sites across the species' ranges supported limited ongoing mixing among the four species with Bayesian clustering and principal component analyses. In contrast, f4-statistics and admixture graphs revealed extensive historical introgression among geographically structured populations. Almost all historical admixture events were among populations west of the Rocky Mountains, and almost all populations west of the Rocky Mountains, excluding island and coastal populations, showed evidence of historical admixture. The inclusion of all four chickadee species proved crucial in differentiating which species were involved in hybridization events to avoid erroneous conclusions. Taken together, the results suggest a complex pattern of divergence with gene flow.

Using recent genetic history to inform conservation options of two Lesser Caymans iguana (Cyclura nubila caymanensis) populations

The Sister Islands rock iguana (Cyclura nubila caymanensis) is critically endangered and endemic to the Caribbean islands Little Cayman and Cayman Brac. The Cayman Brac population and indeed the entire species is under threat from habitat destruction, invasive species, and anthropogenic impacts on the island. We assessed the genetic diversity, estimated effective population sizes, and tested for differentiation of populations between these two islands to inform potential future translocation should this be needed for the Cayman Brac population. Two mitochondrial DNA markers (cytochrome b and NADH subunit 4) and seven DNA microsatellite markers were used to assess the genetic diversity, genetic structure, demographic history, and effective population size of the two iguana populations. Mitochondrial DNA showed no genetic differentiation between populations; however, we found little to moderate divergence with microsatellites. We compared multiple demographic scenarios and revealed that ongoing gene flow is likely. The demographic history implied a significant genetic bottleneck around 10,000 years ago, coinciding with the sea level rise at the close of the last glacial period, and the start of the Holocene. Estimates of current effective population sizes indicate a small-scale number of breeders on each island of similar magnitude to the census mature population size (between 100 and 800 individuals). The relatively low differentiation between populations supports the possible development of active genetic management plans to manage the declining populations of the Sister Islands rock iguana.

A single origin and high genetic diversity of cultivated medicinal herb Glehnia littoralis subsp. littoralis (Apiaceae) deciphered by SSR marker and phenotypic analysis.

Ten SSR markers based on transcriptome sequencing were employed to genotype 231 samples of G. littoralis subsp. littoralis (Apiaceae) from nine cultivated populations and seven wild populations, aiming to assess the genetic diversity and genetic structure, and elucidate the origin of the cultivated populations. Cultivated populations exhibited relatively high genetic diversity (h = 0.441, I = 0.877), slightly lower than that of their wild counterparts (h = 0.491, I = 0.930), likely due to recent domestication and ongoing gene flow between wild and cultivated germplasm. The primary cultivated population in Shandong have the crucial genetic status. A single origin of domestication was inferred through multiple analysis, and wild populations from Liaoning and Shandong are inferred to be potentially the ancestor source for the present cultivated populations. Phenotypic analysis revealed a relatively high heritability of root length across three growth periods (0.683, 0.284, 0.402), with significant correlations observed between root length and petiole length (Pearson correlation coefficient = 0.30, P<0.05), as well as between root diameter and leaf area (Pearson correlation coefficient = 0.36, P<0.01). These parameters can serve as valuable indicators for monitoring the developmental progress of medicinal plants during field management. In summary, this study can shed light on the intricate genetic landscape of G. littoralis subsp. littoralis, providing foundational insights crucial for conservation strategies, targeted breeding initiatives, and sustainable management practices in both agricultural and natural habitats.

Major patterns in the introgression history of Heliconius butterflies

Gene flow between species, although usually deleterious, is an important evolutionary process that can facilitate adaptation and lead to species diversification. It also makes estimation of species relationships difficult. Here, we use the full-likelihood multispecies coalescent (MSC) approach to estimate species phylogeny and major introgression events in Heliconius butterflies from whole-genome sequence data. We obtain a robust estimate of species branching order among major clades in the genus, including the ‘melpomene-silvaniform’ group, which shows extensive historical and ongoing gene flow. We obtain chromosome-level estimates of key parameters in the species phylogeny, including species divergence times, present-day and ancestral population sizes, as well as the direction, timing, and intensity of gene flow. Our analysis leads to a phylogeny with introgression events that differ from those obtained in previous studies. We find that Heliconius aoede most likely represents the earliest-branching lineage of the genus and that ‘silvaniform’ species are paraphyletic within the melpomene-silvaniform group. Our phylogeny provides new, parsimonious histories for the origins of key traits in Heliconius, including pollen feeding and an inversion involved in wing pattern mimicry. Our results demonstrate the power and feasibility of the full-likelihood MSC approach for estimating species phylogeny and key population parameters despite extensive gene flow. The methods used here should be useful for analysis of other difficult species groups with high rates of introgression.

Major patterns in the introgression history of Heliconius butterflies.

Gene flow between species, although usually deleterious, is an important evolutionary process that can facilitate adaptation and lead to species diversification. It also makes estimation of species relationships difficult. Here, we use the full-likelihood multispecies coalescent (MSC) approach to estimate species phylogeny and major introgression events in Heliconius butterflies from whole-genome sequence data. We obtain a robust estimate of species branching order among major clades in the genus, including the 'melpomene-silvaniform' group, which shows extensive historical and ongoing gene flow. We obtain chromosome-level estimates of key parameters in the species phylogeny, including species divergence times, present-day and ancestral population sizes, as well as the direction, timing, and intensity of gene flow. Our analysis leads to a phylogeny with introgression events that differ from those obtained in previous studies. We find that Heliconius aoede most likely represents the earliest-branching lineage of the genus and that 'silvaniform' species are paraphyletic within the melpomene-silvaniform group. Our phylogeny provides new, parsimonious histories for the origins of key traits in Heliconius, including pollen feeding and an inversion involved in wing pattern mimicry. Our results demonstrate the power and feasibility of the full-likelihood MSC approach for estimating species phylogeny and key population parameters despite extensive gene flow. The methods used here should be useful for analysis of other difficult species groups with high rates of introgression.

Scattered differentiation of unlinked loci across the genome underlines ecological divergence of the selfing grass Brachypodium stacei.

Ecological divergence without geographic isolation, as an early speciation process that may lead finally to reproductive isolation through natural selection, remains a captivating topic in evolutionary biology. However, the pattern of genetic divergence underlying this process across the genome may vary between species and mating systems. Here, we present evidence that Brachypodium stacei, an annual and highly selfing grass model species, has undergone sympatric ecological divergence without geographic isolation. Genomic, transcriptomic, and metabolomic analyses together with lab experiments mimicking the two opposite environmental conditions suggest that diploid B. stacei populations have diverged sympatrically in two slopes characterized by distinct biomes at Evolution Canyon I (ECI), Mount Carmel, Israel. Despite ongoing gene flow, primarily facilitated by seed dispersal, the level of gene flow has progressively decreased over time. This local adaptation involves the scattered divergence of many unlinked loci across the total genome that include both coding genes and noncoding regions. Additionally, we have identified significant differential expressions of genes related to the ABA signaling pathway and contrasting metabolome composition between the arid- vs. forest-adapted B. stacei populations in ECI. These results suggest that multiple small loci involved in environmental responses act additively to account for ecological adaptations by this selfing species in contrasting environments.

An evolutionarily distinct ringed seal in the Ilulissat Icefjord.

The Earth's polar regions are low rates of inter- and intraspecific diversification. An extreme mammalian example is the Arctic ringed seal (Pusa hispida hispida), which is assumed to be panmictic across its circumpolar Arctic range. Yet, local Inuit communities in Greenland and Canada recognize several regional variants; a finding supported by scientific studies of body size variation. It is however unclear whether this phenotypic variation reflects plasticity, morphs or distinct ecotypes. Here, we combine genomic, biologging and survey data, to document the existence of a unique ringed seal ecotype in the Ilulissat Icefjord (locally 'Kangia'), Greenland; a UNESCO World Heritage site, which is home to the most productive marine-terminating glacier in the Arctic. Genomic analyses reveal a divergence of Kangia ringed seals from other Arctic ringed seals about 240 kya, followed by secondary contact since the Last Glacial Maximum. Despite ongoing gene flow, multiple genomic regions appear under strong selection in Kangia ringed seals, including candidate genes associated with pelage coloration, growth and osmoregulation, potentially explaining the Kangia seal's phenotypic and behavioural uniqueness. The description of 'hidden' diversity and adaptations in yet another Arctic species merits a reassessment of the evolutionary processes that have shaped Arctic diversity and the traditional view of this region as an evolutionary freezer. Our study highlights the value of indigenous knowledge in guiding science and calls for efforts to identify distinct populations or ecotypes to understand how these might respond differently to environmental change.

Ancestry testing of "Old Tom," a killer whale central to mutualistic interactions with human whalers.

Cooperative hunting between humans and killer whales (Orcinus orca) targeting baleen whales was reported in Eden, New South Wales, Australia, for almost a century. By 1928, whaling operations had ceased, and local killer whale sightings became scarce. A killer whale from the group, known as "Old Tom," washed up dead in 1930 and his skeleton was preserved. How these killer whales from Eden relate to other populations globally and whether their genetic descendants persist today remains unknown. We extracted and sequenced DNA from Old Tom using ancient DNA techniques. Genomic sequences were then compared with a global dataset of mitochondrial and nuclear genomes. Old Tom shared a most recent common ancestor with killer whales from Australasia, the North Atlantic, and the North Pacific, having the highest genetic similarity with contemporary New Zealand killer whales. However, much of the variation found in Old Tom's genome was not shared with these widespread populations, suggesting ancestral rather than ongoing gene flow. Our genetic comparisons also failed to find any clear descendants of Tom, raising the possibility of local extinction of this group. We integrated Traditional Custodian knowledge to recapture the events in Eden and recognize that Indigenous Australians initiated the relationship with the killer whales before European colonization and the advent of commercial whaling locally. This study rectifies discrepancies in local records and provides new insight into the origins of the killer whales in Eden and the history of Australasian killer whales.

A Preliminary mitochondrial cytochrome c oxidase-I-based phylogeographic and phylogenetic analysis of Eurasian Acanthocinus griseus (Coleoptera, Cerambycidae)

Acanthocinus griseus (Fabricius, 1792) (Coleoptera: Cerambycidae, Lamiinae, Acanthocinini) has long been known for its role in the decay process of the wood in the forest ecosystem, and two critical features of the species, inhabiting standing trees and being a vector of pine wood nematodes Bursaphelenchus spp., have been noted recently. Therefore, understanding the current relationships and possible migration scenarios has been further required to assess invasion risks. The present work provided a preliminary comprehension of the phylogenetic relationships of A. griseus based on the mitochondrial cytochrome c oxidase-I (COI) gene region (658 bp), with sequences produced in the present study, from the specimens collected from timberyards, ports and forests of Kocaeli Province, Turkey, and with available sequences in GenBank of inhabitants of Eurasia, and of intercepted specimens in ports. The intraspecific genetic distance of A. griseus was 1.37-0,3%, while the interspecific distance was 10,79-13,37%, except the closeness of an A. griseus haplotype (AGR1) to A. sachalinensis (0,3%) more than its conspecifics (4,71-5,47%). The ML and BI analyses suggested identical topologies. The statistical parsimony network drew a reticular branching diagram without grouping across countries or geographic regions, which addresses ongoing gene flow. Most haplotypes from Turkey were clustered around a central haplotype (AGR11), which may point to a bottleneck effect. A haplotype previously intercepted in USA ports was identical to a haplotype sampled in Kocaeli. The present study suggests that the relationship between A. griseus and A. sachalinensis should be reconsidered from both morphological and molecular points of view. In addition, the possible ongoing intraspecific gene flow within A. griseus might be due to facilitated migration by the international wood trade.

Phylogenomics of the extinct Heath Hen provides support for sex-biased introgression among extant prairie grouse

Rapid divergence and subsequent reoccurring patterns of gene flow can complicate our ability to discern phylogenetic relationships among closely related species. To what degree such patterns may differ across the genome can provide an opportunity to extrapolate better how life history constraints may influence species boundaries. By exploring differences between autosomal and Z (or X) chromosomal-derived phylogenetic patterns, we can better identify factors that may limit introgression despite patterns of incomplete lineage sorting among closely related taxa. Here, using a whole-genome resequencing approach coupled with an exhaustive sampling of subspecies within the recently divergent prairie grouse complex (genus: Tympanuchus), including the extinct Heath Hen (T. cupido cupido), we show that their phylogenomic history differs depending on autosomal or Z-chromosome partitioned SNPs. Because the Heath Hen was allopatric relative to the other prairie grouse taxa, its phylogenetic signature should not be influenced by gene flow. In contrast, all the other extant prairie grouse taxa, except Attwater’s Prairie-chicken (T. c. attwateri), possess overlapping contemporary geographic distributions and have been known to hybridize. After excluding samples that were likely translocated prairie grouse from the Midwest to the eastern coastal states or their resulting hybrids with mainland Heath Hens, species tree analyses based on autosomal SNPs consistently identified a paraphyletic relationship with regard to the Heath Hen with Lesser Prairie-chicken (T. pallidicinctus) sister to Greater Prairie-chicken (T. c. pinnatus) regardless of genic or intergenic partitions. In contrast, species trees based on the Z-chromosome were consistent with Heath Hen sister to a clade that included its conspecifics, Greater and Attwater’s Prairie-chickens (T. c. attwateri). These results were further explained by historic gene flow, as shown with an excess of autosomal SNPs shared between Lesser and Greater Prairie-chickens but not with the Z-chromosome. Phylogenetic placement of Sharp-tailed Grouse (T. phasianellus), however, did not differ among analyses and was sister to a clade that included all other prairie grouse despite low levels of autosomal gene flow with Greater Prairie-chicken. These results, along with strong sexual selection (i.e., male hybrid behavioral isolation) and a lek breeding system (i.e., high variance in male mating success), are consistent with a pattern of female-biased introgression between prairie grouse taxa with overlapping geographic distributions. Additional study is warranted to explore how genomic components associated with the Z-chromosome influence the phenotype and thereby impact species limits among prairie grouse taxa despite ongoing contemporary gene flow.