Effective Population Research Articles

The recombination landscape of the barn owl, from families to populations.

Homologous recombination is a meiotic process that generates diversity along the genome and interacts with all evolutionary forces. Despite its importance, studies of recombination landscapes are lacking due to methodological limitations and limited data. Frequently used approaches include linkage mapping based on familial data that provides sex-specific broad-scale estimates of realized recombination and inferences based on population LD that reveal a more fine scale resolution of the recombination landscape, albeit dependent on the effective population size and the selective forces acting on the population. In this study, we use a combination of these two methods to elucidate the recombination landscape for the Afro-European barn owl (Tyto alba). We find subtle differences in crossover placement between sexes that leads to differential effective shuffling of alleles. LD based estimates of recombination are concordant with family-based estimates and identify large variation in recombination rates within and among linkage groups. Larger chromosomes show variation in recombination rates, while smaller chromosomes have a universally high rate which shapes the diversity landscape. We find that recombination rates are correlated with gene content, genetic diversity and GC content. We find no conclusive differences in the recombination landscapes between populations. Overall, this comprehensive analysis enhances our understanding of recombination dynamics, genomic architecture, and sex-specific variation in the barn owl, contributing valuable insights to the broader field of avian genomics.

Repeated evolution on oceanic islands: comparative genomics reveals species-specific processes in birds

Understanding the interplay between genetic drift, natural selection, gene flow, and demographic history in driving phenotypic and genomic differentiation of insular populations can help us gain insight into the speciation process. Comparing patterns across different insular taxa subjected to similar selective pressures upon colonizing oceanic islands provides the opportunity to study repeated evolution and identify shared patterns in their genomic landscapes of differentiation. We selected four species of passerine birds (Common Chaffinch Fringilla coelebs/canariensis, Red-billed Chough Pyrrhocorax pyrrhocorax, House Finch Haemorhous mexicanus and Dark-eyed/island Junco Junco hyemalis/insularis) that have both mainland and insular populations. Changes in body size between island and mainland populations were consistent with the island rule. For each species, we sequenced whole genomes from mainland and insular individuals to infer their demographic history, characterize their genomic differentiation, and identify the factors shaping them. We estimated the relative (Fst) and absolute (dxy) differentiation, nucleotide diversity (π), Tajima’s D, gene density and recombination rate. We also searched for selective sweeps and chromosomal inversions along the genome. All species shared a marked reduction in effective population size (Ne) upon island colonization. We found diverse patterns of differentiated genomic regions relative to the genome average in all four species, suggesting the role of selection in island-mainland differentiation, yet the lack of congruence in the location of these regions indicates that each species evolved differently in insular environments. Our results suggest that the genomic mechanisms involved in the divergence upon island colonization—such as chromosomal inversions, and historical factors like recurrent selection—differ in each species, despite the highly conserved structure of avian genomes and the similar selective factors involved. These differences are likely influenced by factors such as genetic drift, the polygenic nature of fitness traits and the action of case-specific selective pressures.

Gene flow stimulates recovery of reproductive fitness in a captive bred insect

Abstract Captive breeding can be a useful tool for the management of threatened species, but such programs often begin with a bottleneck which may lower reproductive fitness by increasing inbreeding and allowing deleterious alleles to increase in frequency by reducing effective population size. Dryococelus australis, the Lord Howe Island stick insect, is a critically endangered insect that has been bred at the Melbourne Zoo in Melbourne, Australia, since shortly after the species was rediscovered in 2001. We analysed a long‐term dataset of phenotypic measurements from this captive breeding program to determine whether reproductive fitness has declined in captivity. We found a clear signal of decline in direct (egg hatching success) and indirect (egg and nymph size) fitness indicators over time. We compared a captive line descended from the original program founders to a new hybrid line that has recent wild ancestry. The hybrid line showed an immediate improvement in egg hatch rate, suggesting the potential for genetic rescue. Egg and nymph size did not show as dramatic a change, although this line had only existed for just over a single generation at the time of data collection. These results argue strongly for the regular sourcing of new genetic material from the wild D. australis population to counteract fitness declines in captivity. Aside from benefiting the captive population, this would also improve the prospects of establishing new wild populations in the future, using individuals sourced from captivity.

Genomic architecture in social insects is more strongly associated with phylogeny than social behavior

Abstract The evolution of sociality in insects has been predicted to reduce effective population sizes, in turn leading to changes in genome architecture, including higher recombination rates, larger genomes, increased GC-biased gene conversion (gBGC), and greater intragenomic variation in GC content to maintain castes through differential methylation. As the number of sequenced insect genomes continues to grow, it remains an open question which, if any, of these genomic features are consistent across social insect genomes. A major challenge to determining such commonalities has been the lack of phylogenetically controlled analyses across independent origins of sociality. Of the 15 Hymenoptera species for which recombination rate was available, social species had higher rates of recombination. Next, we conducted a broader analysis of genome architecture by analyzing genome assemblies for 435 species of Hymenoptera and 8 species of Blattodea to test if GC content, genome size, distribution of CpG sites or codon bias repeatedly differed between social and nonsocial species. Overall, there was little support for predictable changes in genome architecture associated with sociality across Hymenoptera, after accounting for phylogenetic relationships. However, we found a significant negative relationship between sociality and GC content within the family Apidae and a significant negative relationship between sociality and genome size within the family Halictidae. In all, these results suggest that unique origins of social behavior may produce unique trends in genomic architecture. Our study highlights the need to examine genome architecture across independent origins of social behavior.

Restricted inclusion of wild broodstock at a large hatchery does not result in detectable genetic differentiation in a supplemented coho salmon (Oncorhynchus kisutch) population

Hatchery production is common in salmonid management for harvest and conservation. Many hatcheries employ integrated broodstock programs, where wild-origin fish are included as broodstock and uni- or bi-directional gene flow between wild and hatchery components of the population is encouraged. Such approaches often assume that opportunistically obtained wild fish meet the genetic goals of minimizing hatchery–wild differentiation and maintaining genetic diversity. This may be incorrect if fine-scale spatial genetic structure exists. Here we investigate the population genetic consequences of such hatchery operations in coho salmon ( Oncorhynchus kisutch) in a small river system featuring a large integrated broodstock program. We do so using 11 082 SNPs scored in wild-origin and hatchery-origin fish collected throughout the system. We found no evidence for genetic differentiation between hatchery-origin and wild-origin fish, no evidence of lowered genetic diversity in hatchery-origin fish, and no evidence for genetic differentiation among fish sampled throughout the river system. In addition, we did not detect inbreeding. Collectively, these results are consistent with current practices meeting integrated hatchery program goals of adequately sampling the genetic diversity present in wild-origin fish, although they may slightly reduce the effective population size of the combined population.

Characterizing local pig breeds as reservoirs for the domestic pig genetic variability worldwide via contributions to gene diversity and allelic richness.

Contributions to gene diversity and allelic richness were computed in a total of 2,260 domestic pig genotypes, sharing 53,626 autosomal SNPs, belonging to 98 pig subpopulations worldwide (41 Asian, 696 genotypes; 20 American, 262 genotypes; and 37 European, 686 genotypes), using 616 pig samples belonging to six different Cosmopolitan pig breeds as an outgroup, to ascertain if local pig subpopulation can be considered reservoirs of genetic diversity for the whole domestic pig species worldwide. Assessments were carried out for the whole dataset and separately for the American-European and Asian subsets. Effective population size was computed at the subpopulation level using molecular coancestry and linkage disequilibrium information to ensure that estimates of contributions to diversity were not affected by demographic issues. Most American and European pig subpopulations tended to have favorable contributions to both gene diversity and allelic richness. However, contributions to allelic richness were more consistent than those obtained for gene diversity, whether the computations are performed using either the whole dataset or the American-Asian subset, suggesting that allelic richness can be a key parameter to identify putative reservoirs for the species. The Asian pig subpopulations never contributed favorably to the allelic richness of the domestic pig metapopulation. Although these results can partially be explained by the highly divergent origins of the American-European and the Asian pig subpopulations, it cannot be discarded that the results obtained for the Asian subpopulations are biased due to a worse calling performance of the pig SNP arrays used for genotyping. The use of other potentially less biased sources of genotypic information is advisable to compare the Asian and American-European pig subpopulations genetic diversity.

Comparing genomic studies in animal breeding and human genetics: Focus on disease-related traits in livestock.

Genomic studies of diseases can be divided into two types: (1) analyses that reveal causal genes by focusing on linkage disequilibrium between observed and causal variants and (2) those that simultaneously assess numerous genetic markers to estimate the polygenic effects of a particular genomic region or entire genome. The field of human genetics has emphasized the discovery of causal genes, but these represent only a fraction of the total genetic variance. Therefore, alternative approaches, such as the polygenic risk score, which estimates the genetic risk for a given trait or disease on the basis of all genetic markers (rather than on known causal variants only), have begun to garner attention. In many respects, these human genetic methods are similar to those originally developed for the estimation of breeding values (i.e., total additive genetic effects) in livestock. However, despite these similarities in methods, the fields of human and animal genetics still differ markedly in terms of research objectives, target populations, and other characteristics. For example, livestock populations have continually been selected and inbred throughout their history; consequently, their effective population size has shrunk and preferred genes (such as those influencing disease resistance and production traits) have accumulated in the modern breeding populations. By examining the characteristics of these two fields, particularly from the perspectives of disease and disease resistance, this review aims to improve understanding of the intrinsic differences between genomic studies using human compared with livestock populations.

Abundant genetic variation is retained in many laboratory schistosome populations.

Schistosomes are obligately sexual blood flukes that can be maintained in the laboratory using freshwater snails as intermediate and rodents as definitive hosts. The genetic composition of laboratory schistosome populations is poorly understood: whether genetic variation has been purged due to serial inbreeding or retained is unclear. We sequenced 19 - 24 parasites from each of five laboratory Schistosoma mansoni populations and compared their genomes with published exome data from four S. mansoni field populations. We found abundant genomic variation (0.897 - 1.22 million variants) within laboratory populations: these retained on average 49% (π = 3.27e-04 - 8.94e-04) of the nucleotide diversity observed in the four field parasite populations (π = 1.08e-03 - 2.2e-03). However, the pattern of variation was very different in laboratory and field populations. Tajima's D was positive in all laboratory populations except SmBRE, indicative of recent population bottlenecks, but negative in all field populations. Current effective population size estimates of laboratory populations were lower (2 - 258) compared to field populations (3,174 - infinity). The distance between markers at which linkage disequilibrium (LD) decayed to 0.5 was longer in laboratory populations (59 bp - 180 kb) compared to field populations (9 bp - 9.5 kb). SmBRE was the least variable; this parasite also shows low fitness across the lifecycle, consistent with inbreeding depression. The abundant genetic variation present in most laboratory schistosome populations has several important implications: (i) measurement of parasite phenotypes, such as drug resistance, using laboratory parasite populations will determine average values and underestimate trait variation; (ii) genome-wide association studies (GWAS) can be conducted in laboratory schistosome populations by measuring phenotypes and genotypes of individual worms; (iii) genetic drift may lead to divergence in schistosome populations maintained in different laboratories. We conclude that the abundant genetic variation retained within many laboratory schistosome populations can provide valuable, untapped opportunities for schistosome research.

Life's a ditch: demographic history and environmental factors shape fine-scale local adaptation within small populations of brook trout

Many studies have investigated the loss of adaptive potential in endangered or exploited species experiencing recent population declines. Less research has studied adaptive genomic variation in small populations known to have persisted for long periods, despite the unique contribution that such populations provide for determining mechanisms underlying population persistence in evolutionary and conservation modeling. Small populations of Brook trout (Salvelinus fontinalis) have persisted in Cape Race, Newfoundland for >12,000 years. We used genotyping-by-sequencing data to investigate the demographic history and adaptive genomic variation of 26 populations with effective population sizes (Ne) ranging from 11 to 442, and to explore mechanisms underlying long-term persistence. We show that all populations experienced demographic declines following postglacial colonization but have remained in their current, small Ne state for thousands of years. We also reveal greater homozygosity in adaptive alleles within the smallest populations and found signatures of adaptive divergence in small populations relating to several abiotic and biotic factors. Our study illustrates how the demographic history of a species can influence the adaptive dynamics of small populations persisting over long time periods.

Advancing equine genomics: the development of a high density Axiom_Ashwa SNP chip for Indian horses and ponies.

The unique horse and pony breeds of India are declining at an alarming rate. These horses have been integral to the Indian culture and customs for centuries and represent a valuable genetic resource. It is imperative to harness the potential of this equine genetic resource that urgently needs conservation. The study highlights the design and development of a high density SNP array, the Axiom_Ashwa to aid in the genetic analysis and conservation efforts for Indian horse and pony breeds. With 613,950 SNPs, this chip offers extensive genome coverage having an average inter-marker distance of 4kb. The Axiom_Ashwa has been validated on a larger set of diverse indigenous samples as well as Thoroughbreds, demonstrating a high call rate of 99.4% and robustness for genotyping indigenous breeds. Linkage disequilibrium (LD) analysis showed higher average LD in Indian breeds compared to exotic breeds, suggesting a limited effective population size and recent bottlenecks. Phylogenetic and population stratification analyses using PCA and DAPC clearly distinguished horses, ponies and Thoroughbreds, confirming the efficacy of the Axiom_Ashwa chip. These findings underscore the urgent need for conservation efforts for Indian horse breeds, which have experienced significant drop in population size. The Axiom_Ashwa SNP chip offers advantages such as cost-effectiveness and high throughput, providing a more accurate genetic representation of Indian horses.

Repeated horizontal acquisition of lagriamide-producing symbionts in Lagriinae beetles.

Microbial symbionts associate with multicellular organisms on a continuum from facultative associations to mutual codependency. In the oldest intracellular symbioses there is exclusive vertical symbiont transmission, and co-diversification of symbiotic partners over millions of years. Such symbionts often undergo genome reduction due to low effective population sizes, frequent population bottlenecks, and reduced purifying selection. Here, we describe multiple independent acquisition events of closely related defensive symbionts followed by genome erosion in a group of Lagriinae beetles. Previous work in Lagria villosa revealed the dominant genome-eroded symbiont of the genus Burkholderia produces the antifungal compound lagriamide, protecting the beetle's eggs and larvae from antagonistic fungi. Here, we use metagenomics to assemble 11 additional genomes of lagriamide-producing symbionts from seven different host species within Lagriinae from five countries, to unravel the evolutionary history of this symbiotic relationship. In each host, we detected one dominant genome-eroded Burkholderia symbiont encoding the lagriamide biosynthetic gene cluster. However, we did not find evidence for host-symbiont co-diversification, or for monophyly of the lagriamide-producing symbionts. Instead, our analyses support a single ancestral acquisition of the gene cluster followed by at least four independent symbiont acquisitions and subsequent genome erosion in each lineage. By contrast, a clade of plant-associated relatives retained large genomes but secondarily lost the lagriamide gene cluster. Our results, therefore, reveal a dynamic evolutionary history with multiple independent symbiont acquisitions characterized by a high degree of specificity, and highlight the importance of the specialized metabolite lagriamide for the establishment and maintenance of this defensive symbiosis.

Phylodynamic Structure in the Botswana HIV Epidemic.

Background Studying viral sequences can provide insights into the structure of host contact networks through which the virus is transmitted. Uncovering the population structure of the HIV-1 epidemic in Botswana will help optimise public health interventions and may identify hidden sub-epidemics. We sought to determine the phylodynamic structure of the Botswana HIV-1 epidemic from viral sequence genetic data. Methods The Botswana Combination Prevention Project (BCPP) randomly sampled 20% of households in 30 villages in Botswana between 2013-2018 and tested for HIV-1. Extensive demographic data were collected from all participants and next-generation full-genome HIV-1 sequences were generated from HIV-1 positive participants (n = 4,164), 78% of whom were on antiretroviral treatment (ART). We inferred the stage of infection (< or > 1 year) among HIV-1 cases based on nucleotide diversity and clinical data using a previously trained machine learning model. We then reconstructed time-resolved gag and pol phylogenies from sequences, other Botswana cohorts and publicly available sequences that were genetically close to those from Botswana. We statistically explored phylogenies for partitions with diverging patterns of coalescence, indicating sub-epidemics, and estimated viral effective population size through time, a measure of viral incidence, for each partition. Finally, we compared the demographic makeup, clinical and geographic characteristics across partitions using χ2, ANOVA tests and Tukey analysis. Results We identified three partitions of time-resolved gag and pol phylogenies, revealing divergent patterns of coalescence and HIV-1 transmission. In both gag and pol phylogenies, partitions with persistent growth and transmission were characterised by lower treatment coverage and more recent infections when compared to other partitions. The Southern and South East regions of Botswana were over-represented in the fast-growing partitions. Conclusion Our findings suggest that transmission is slowing in segments of the population that have high ART coverage. However, recent infections are over-represented in ongoing sub-epidemics. The phylodynamic structure suggests that there are districts with higher growth and prioritising these in the deployment of public health interventions might curb new infections. Nonetheless the high mobility of Botswana residents should be taken into consideration in implementing effective interventions to combat HIV-1.

Resilience of genetic diversity in forest trees over the Quaternary

The effect of past environmental changes on the demography and genetic diversity of natural populations remains a contentious issue and has rarely been investigated across multiple, phylogenetically distant species. Here, we perform comparative population genomic analyses and demographic inferences for seven widely distributed and ecologically contrasting European forest tree species based on concerted sampling of 164 populations across their natural ranges. For all seven species, the effective population size, Ne, increased or remained stable over many glacial cycles and up to 15 million years in the most extreme cases. Surprisingly, the drastic environmental changes associated with the Pleistocene glacial cycles have had little impact on the level of genetic diversity of dominant forest tree species, despite major shifts in their geographic ranges. Based on their trajectories of Ne over time, the seven tree species can be divided into three major groups, highlighting the importance of life history and range size in determining synchronous variation in genetic diversity over time. Altogether, our results indicate that forest trees have been able to retain their evolutionary potential over very long periods of time despite strong environmental changes.

Population Genomics of Adaptive Radiations: Exceptionally High Levels of Genetic Diversity and Recombination in an Endemic Spider From the Canary Islands.

The spider genus Dysdera has undergone a remarkable diversification in the oceanic archipelago of the Canary Islands, with ~60 endemic species having originated during the 20 million years since the origin of the archipelago. This evolutionary radiation has been accompanied by substantial dietary shifts, often characterised by phenotypic modifications encompassing morphological, metabolic and behavioural changes. Hence, these endemic spiders represent an excellent model for understanding the evolutionary drivers and to pinpoint the genomic determinants underlying adaptive radiations. Recently, we achieved the first chromosome-level genome assembly of one of the endemic species, D. silvatica, providing a high-quality reference sequence for evolutionary genomics studies. Here, we conducted a low coverage-based resequencing study of a natural population of D. silvatica from La Gomera island. Taking advantage of the new high-quality genome, we characterised genome-wide levels of nucleotide polymorphism, divergence and linkage disequilibrium, and inferred the demographic history of this population. We also performed comprehensive genome-wide scans for recent positive selection. Our findings uncovered exceptionally high levels of nucleotide diversity and recombination in this geographically restricted endemic species, indicative of large historical effective population sizes. We also identified several candidate genomic regions that are potentially under positive selection, highlighting relevant biological processes, such as vision and nitrogen extraction as potential adaptation targets. These processes may ultimately drive species diversification in this genus. This pioneering study of spiders that are endemic to an oceanic archipelago lays the groundwork for broader population genomics analyses aimed at understanding the genetic mechanisms driving adaptive radiation in island ecosystems.

Too big to purge: persistence of deleterious Mutations in Island populations of the European Barn Owl (Tyto alba).

A key aspect of assessing the risk of extinction/extirpation for a particular wild species or population is the status of inbreeding, but the origin of inbreeding and the current mutational load are also two crucial factors to consider when determining survival probability of a population. In this study, we used samples from 502 barn owls from continental and island populations across Europe, with the aim of quantifying and comparing the level of inbreeding between populations with differing demographic histories. In addition to comparing inbreeding status, we determined whether inbreeding is due to non-random mating or high co-ancestry within the population. We show that islands have higher levels of inbreeding than continental populations, and that this is mainly due to small effective population sizes rather than recent consanguineous mating. We assess the probability that a region is autozygous along the genome and show that this probability decreased as the number of genes present in that region increased. Finally, we looked for evidence of reduced selection efficiency and purging in island populations. Among island populations, we found an increase in numbers of both neutral and deleterious minor alleles, possibly as a result of drift and decreased selection efficiency but we found no evidence of purging.

Genomic signatures of inbreeding and mutation load in tree ferns.

Ferns (Pteridophyta), as the second largest group of vascular plants, play important roles in ecosystem functioning. Homosporous ferns exhibit a remarkable range of mating systems, from extreme inbreeding to obligate outcrossing, which may have significant evolutionary and ecological implications. Despite their significance, the impact of genome-wide inbreeding on genetic diversity and mutation load within the fern lineage remain largely unexplored. In this study, we utilized whole-genome sequencing to investigate the genomic signatures of inbreeding and genetic load in three Alsophila tree fern species. Our analysis revealed extremely high inbreeding in A. spinulosa, in contrast to the predominantly outcrossing observed in A. costularis and A. latebrosa. This difference likely reflects divergent mating systems and demographic histories. Consistent with its extreme inbreeding propensity, A. spinulosa exhibits reduced genetic diversity and a pronounced decline in effective population size. Comparison of genetic load revealed an overall reduction in deleterious mutations in the highly inbred A. spinulosa, highlighting that long-term inbreeding may have contributed to the purging of strongly deleterious mutations, thereby prolonging the survival of A. spinulosa. Despite this, however, A. spinulosa carries a substantive realized genetic load that may potentially instigate future fitness decline. Our findings illuminate the complex evolutionary interplay between inbreeding and mutation load in homosporous ferns, yielding insights with important implications for the conservation and management of these species.

Population connectivity and size reductions in the Anthropocene: the consequence of landscapes and historical bottlenecks in white forsythia fragmented habitats

BackgroundWhite forsythia (Abeliophyllum distichum) is an endangered Korean Peninsula endemic that has been subjected to recent population genomics studies using SNPs via RAD sequencing. Here, we primarily employed the often underutilized haplotype information from RAD loci to further describe the species’ previously uninvestigated haplotype-based genomic variation and structure, and genetic-geographic characteristics and gene flow patterns among its five earlier identified genetic groups. We also inferred the time of past events that may have impacted the effective population size of these groups, as well as the species’ potential future distribution amidst the warming climate and anthropogenic threats.ResultsOur findings emphasized the recognition of the species’ regional patterns of genetic structure, and the role of topography and its associated gene flow patterns as some of the possible factors that may have influenced the species’ present-day fragmented population distribution. The inferred bottleneck events during the Anthropocene, some of which aligned with the time of historical catastrophic events on the Peninsula (e.g., the Korean War), were revealed to have contributed to the generally low effective population size of its five lineages, particularly those with marginal distributional range. Future distribution under both optimistic and pessimistic climatic scenarios suggests unlikely suitable habitats for these populations to expand from their current range limits, at least in the next 80 years.ConclusionsThe small effective population size and landscape-driven limited gene flow among white forsythia populations will remain a big challenge for the conservation management of the species’ already fragmented population distribution. To help mitigate these impacts, the merging of various research approaches and the use of genomic data to their full potential is recommended to provide the optimized knowledge-based tools for the conservation of this endangered species, and other similar plants under pressure.

Purifying Selection Influences the Comparison of Heterozygosities between Populations.

Heterozygosity is a fundamental measure routinely used to compare between populations to infer the level of genetic variation and their relative effective population sizes. However, such comparison is highly influenced by the magnitude of selection pressure on the genomic regions used. Using over 2 million Single Nucleotide Variants (SNVs) from chimpanzee and mouse populations, this study shows that the heterozygosities estimated using neutrally evolving sites of large populations were two times higher than those of small populations. However, this difference was only ~1.6 times for the heterozygosities estimated using nonsynonymous sites. This suggests an excess in the nonsynonymous heterozygosities due to the segregation of deleterious variants in small populations. This excess in the nonsynonymous heterozygosities of the small populations was estimated to be 23-31%. Further analysis revealed that the magnitude of the excess is modulated by effective population size (Ne) and selection intensity (s). Using chimpanzee populations, this investigation found that the excess in nonsynonymous diversity in the small population was little (6%) when the difference between the Ne values of large and small populations was small (2.4 times). Conversely, this was high (23%) when the difference in Ne was large (5.9 times). Analysis using mouse populations showed that the excess in the nonsynonymous diversity of highly constrained genes of the small population was much higher (38%) than that observed for the genes under relaxed selective constraints (21%). Similar results were observed when the expression levels of genes were used as a proxy for selection intensity. These results emphasize the use of neutral regions, less constrained genes, or lowly expressed genes when comparing the heterozygosities between populations.

Inference of Phylogenetic Networks from Sequence Data using Composite Likelihood.

While phylogenies have been essential in understanding how species evolve, they do not adequately describe some evolutionary processes. For instance, hybridization, a common phenomenon where interbreeding between two species leads to formation of a new species, must be depicted by a phylogenetic network, a structure that modifies a phylogenetic tree by allowing two branches to merge into one, resulting in reticulation. However, existing methods for estimating networks become computationally expensive as the dataset size and/or topological complexity increase. The lack of methods for scalable inference hampers phylogenetic networks from being widely used in practice, despite accumulating evidence that hybridization occurs frequently in nature. Here, we propose a novel method, PhyNEST (Phylogenetic Network Estimation using SiTe patterns), that estimates binary, level-1 phylogenetic networks with a fixed, user-specified number of reticulations directly from sequence data. By using the composite likelihood as the basis for inference, PhyNEST is able to use the full genomic data in a computationally tractable manner, eliminating the need to summarize the data as a set of gene trees prior to network estimation. To search network space, PhyNEST implements both hill climbing and simulated annealing algorithms. PhyNEST assumes that the data are composed of coalescent independent sites that evolve according to the Jukes-Cantor substitution model and that the network has a constant effective population size. Simulation studies demonstrate that PhyNEST is often more accurate than two existing composite likelihood summary methods (SNaQ and PhyloNet) and that it is robust to at least one form of model misspecification (assuming a less complex nucleotide substitution model than the true generating model). We applied PhyNEST to reconstruct the evolutionary relationships among Heliconius butterflies and Papionini primates, characterized by hybrid speciation and widespread introgression, respectively. PhyNEST is implemented in an open-source Julia package and is publicly available at https://github.com/sungsik-kong/PhyNEST.jl.

Rapid evolution of mitochondrion-related genes in haplodiploid arthropods

BackgroundMitochondrial genes and nuclear genes cooperate closely to maintain the functions of mitochondria, especially in the oxidative phosphorylation (OXPHOS) pathway. However, mitochondrial genes among arthropod lineages have dramatic evolutionary rate differences. Haplodiploid arthropods often show fast-evolving mitochondrial genes. One hypothesis predicts that the small effective population size of haplodiploid species could enhance the effect of genetic drift leading to higher substitution rates in mitochondrial and nuclear genes. Alternatively, positive selection or compensatory changes in nuclear OXPHOS genes could lead to the fast-evolving mitochondrial genes. However, due to the limited number of arthropod genomes, the rates of evolution for nuclear genes in haplodiploid species, besides hymenopterans, are largely unknown. To test these hypotheses, we used data from 76 arthropod genomes, including 5 independently evolved haplodiploid lineages, to estimate the evolutionary rates and patterns of gene family turnover of mitochondrial and nuclear genes.ResultsWe show that five haplodiploid lineages tested here have fast-evolving mitochondrial genes and fast-evolving nuclear genes related to mitochondrial functions, while nuclear genes not related to mitochondrion showed no significant evolutionary rate differences. Among hymenopterans, bees and ants show faster rates of molecular evolution in mitochondrial genes and mitochondrion-related nuclear genes than sawflies and wasps. With genome data, we also find gene family expansions and contractions in mitochondrion-related genes of bees and ants.ConclusionsOur results reject the small population size hypothesis in haplodiploid species. A combination of positive selection and compensatory changes could lead to the observed patterns in haplodiploid species. The elevated evolutionary rates in OXPHOS complex 2 genes of bees and ants suggest a unique evolutionary history of social hymenopterans.