Comparative population genomics of latitudinal variation in Drosophila simulans and Drosophila melanogaster

Examples of clinal variation in phenotypes and genotypes across latitudinal transects have served as important models for understanding how spatially varying selection and demographic forces shape variation within species. Here, we examine the selective and demographic contributions to latitudinal variation through the largest comparative genomic study to date of Drosophila simulans and Drosophila melanogaster, with genomic sequence data from 382 individual fruit flies, collected across a spatial transect of 19 degrees latitude and at multiple time points over 2 years. Consistent with phenotypic studies, we find less clinal variation in D. simulans than D. melanogaster, particularly for the autosomes. Moreover, we find that clinally varying loci in D. simulans are less stable over multiple years than comparable clines in D. melanogaster. D. simulans shows a significantly weaker pattern of isolation by distance than D. melanogaster and we find evidence for a stronger contribution of migration to D. simulans population genetic structure. While population bottlenecks and migration can plausibly explain the differences in stability of clinal variation between the two species, we also observe a significant enrichment of shared clinal genes, suggesting that the selective forces associated with climate are acting on the same genes and phenotypes in D. simulans and D. melanogaster.     

Host‐associated genomic differentiation in congeneric butterflies: now you see it,now you do not

Ecotypic variation among populations may become associated with widespread genomic differentiation, but theory predicts that this should happen only under particular conditions of gene flow, selection and population size. In closely related species, we might expect the strength of host‐associated genomic differentiation (HAD) to be correlated with the degree of phenotypic differentiation in host‐adaptive traits. Using microsatellite and Amplified Fragment Length Polymorphism (AFLP) markers, and controlling for isolation by distance between populations, we sought HAD in two congeneric species of butterflies with different degrees of host plant specialization. Prior work on Euphydryas editha had shown strong interpopulation differentiation in host‐adapted traits, resulting in incipient reproductive isolation among host‐associated ecotypes. We show here that Euphydryas aurinia had much weaker host‐associated phenotypic differentiation. Contrary to our expectations, we detected HAD in Euphydryas aurinia, but not in E. editha. Even within an E. aurinia population that fed on both hosts, we found weak but significant sympatric HAD that persisted in samples taken 9 years apart. The finding of significantly stronger HAD in the system with less phenotypic differentiation may seem paradoxical. Our findings can be explained by multiple factors, ranging from differences in dispersal or effective population size, to spatial variation in genomic or phenotypic traits and to structure induced by past histories of host‐adapted populations. Other infrequently measured factors, such as differences in recombination rates, may also play a role. Our result adds to recent work as a further caution against assumptions of simple relationships between genomic and adaptive phenotypic differentiation.     

Whole‐genome resequencing reveals the pleistocene temporal dynamics of Branchiostoma belcheri and Branchiostoma floridae populations

Global climatic fluctuations governed the ancestral demographic histories of species and contributed to place the current population status into a more extensive ecological and evolutionary context. Genetic variations will leave unambiguous signatures in the patterns of intraspecific genetic variation in extant species since the genome of each individual is an imperfect mosaic of the ancestral genomes. Here, we report the genome sequences of 20 Branchiostoma individuals by whole‐genome resequencing strategy. We detected over 140 million genomic variations for each Branchiostoma individual. In particular, we applied the pairwise sequentially Markovian coalescent (PSMC) method to estimate the trajectories of changes in the effective population size (N_e) of Branchiostoma population during the Pleistocene. We evaluated the threshold of sequencing depth for proper inference of demographic histories using PSMC was ≥25×. The PSMC results highlight the role of historical global climatic fluctuations in the long‐term population dynamics of Branchiostoma. The inferred ancestral N_e of the Branchiostoma belcheri populations from Zhanjiang and Xiamen (China) seawaters was different in amplitude before the first (mutation rate = 3 × 10^?9) or third glaciation (mutation rate = 9 × 10^?9) of the Pleistocene, indicating that the two populations most probably started to evolve in isolation in their respective seas after the first or third glaciation of the Pleistocene. A pronounced population bottleneck coinciding with the last glacial maximum was observed in all Branchiostoma individuals, followed by a population expansion occurred during the late Pleistocene. Species that have experienced long‐term declines may be especially vulnerable to recent anthropogenic activities. Recently, the industrial pollution and the exploitation of sea sand have destroyed the harmonious living environment of amphioxus species. In the future, we need to protect the habitat of Branchiostoma and make full use of these detected genetic variations to facilitate the functional study of Branchiostoma for adaptation to local environments.     

Contrasting Demographic Structure of Short‐ and Long‐lived Pioneer Tree Species on Amazonian Forest Edges

Although tropical forests have been rapidly converted into human‐modified landscapes, tree species response to forest edges remains poorly examined. In this study, we addressed four pioneer tree species to document demographic shifts experienced by this key ecological group and make inferences about pioneer response to forest edges. All individuals with dbh ≥ 1 cm of two short‐lived (Bellucia grossularioides and Cecropia sciadophylla) and two long‐lived species (Goupia glabra and Laetia procera) were sampled in 20 1‐ha forest edge plots and 20 1‐ha forest interior plots in Oiapoque and Manaus, Northeast and Central Amazon, respectively. As expected, pioneer stem density with dbh ≥ 1 cm increased by around 10–17‐fold along forest edges regardless of species, lifespan, and study site. Edge populations of long‐lived pioneers presented 84–94 percent of their individuals in sapling/subadult size classes, whereas edge populations of short‐lived pioneers showed 56–97 percent of their individuals in adult size classes. These demographic biases were associated with negative and positive net adult recruitment of long‐ and short‐lived pioneers, respectively. Our population‐level analyses support three general statements: (1) native pioneer tree species proliferate along forest edges (i.e., increased density), at least in terms of non‐reproductive individuals; (2) pioneer response to edge establishment is not homogeneous as species differ in terms of demographic structure and net adult recruitment; and (3) some pioneer species, particularly long‐lived ones, may experience population decline due to adult sensitivity to edge‐affected habitats.     

Genetic changes in a novel breeding population of Brassica napus synthesized from hundreds of crosses between B. rapa and B. carinata

Introgression of genomic variation between and within related crop species is a significant evolutionary approach for population differentiation, genome reorganization and trait improvement. Using the Illumina Infinium Brassica 60K SNP array, we investigated genomic changes in a panel of advanced generation new‐type Brassica napus breeding lines developed from hundreds of interspecific crosses between 122 Brassica rapa and 74 Brassica carinata accessions, and compared them with representative accessions of their three parental species. The new‐type B. napus population presented rich genetic diversity and abundant novel genomic alterations, consisting of introgressions from B. rapa and B. carinata, novel allelic combinations, reconstructed linkage disequilibrium patterns and haplotype blocks, and frequent deletions and duplications (nonrandomly distributed), particularly in the C subgenome. After a much shorter, but very intensive, selection history compared to traditional B. napus, a total of 15 genomic regions with strong selective sweeps and 112 genomic regions with putative signals of selective sweeps were identified. Some of these regions were associated with important agronomic traits that were selected for during the breeding process, while others were potentially associated with restoration of genome stability and fertility after interspecific hybridization. Our results demonstrate how a novel method for population‐based crop genetic improvement can lead to rapid adaptation, restoration of genome stability and positive responses to artificial selection.     

Without management interventions,endemic wet‐sclerophyll forest is transitioning to rainforest in World Heritage listed K’gari (Fraser Island), Australia

Wet‐sclerophyll forests are unique ecosystems that can transition to dry‐sclerophyll forests or to rainforests. Understanding of the dynamics of these forests for conservation is limited. We evaluated the long‐term succession of wet‐sclerophyll forest on World Heritage listed K'gari (Fraser Island)—the world's largest sand island. We recorded the presence and growth of tree species in three 0.4 hectare plots that had been subjected to selective logging, fire, and cyclone disturbance over 65 years, from 1952 to 2017. Irrespective of disturbance regimes, which varied between plots, rainforest trees recruited at much faster rates than the dominant wet‐sclerophyll forest trees, narrowly endemic species Syncarpia hillii and more common Lophostemon confertus. Syncarpia hillii did not recruit at the plot with the least disturbance and recruited only in low numbers at plots with more prominent disturbance regimes in the ≥10 cm at breast height size. Lophostemon confertus recruited at all plots but in much lower numbers than rainforest trees. Only five L. confertus were detected in the smallest size class (<10 cm diameter) in the 2017 survey. Overall, we find evidence that more pronounced disturbance regimes than those that have occurred over the past 65 years may be required to conserve this wet‐sclerophyll forest, as without intervention, transition to rainforest is a likely trajectory. Fire and other management tools should therefore be explored, in collaboration with Indigenous landowners, to ensure conservation of this wet‐sclerophyll forest.     

Ecological change predicts population dynamics and genetic diversity over 120 000 years

While ecological effects on short‐term population dynamics are well understood, their effects over millennia are difficult to demonstrate and convincing evidence is scant. Using coalescent methods, we analysed past population dynamics of three lizard species (Psammodromus hispanicus, P. edwardsianus, P. occidentalis) and linked the results with climate change data covering the same temporal horizon (120 000 years). An increase in population size over time was observed in two species, and in P. occidentalis, no change was observed. Temporal changes in temperature seasonality and the maximum temperature of the warmest month were congruent with changes in population dynamics observed for the three species and both variables affected population density, either directly or indirectly (via a life‐history trait). These results constitute the first solid link between ecological change and long‐term population dynamics. The results moreover suggest that ecological change leaves genetic signatures that can be retrospectively traced, providing evidence that ecological change is a crucial driver of genetic diversity and speciation.     

Whole‐genome resequencing uncovers molecular signatures of natural and sexual selection in wild bighorn sheep

The identification of genes influencing fitness is central to our understanding of the genetic basis of adaptation and how it shapes phenotypic variation in wild populations. Here, we used whole‐genome resequencing of wild Rocky Mountain bighorn sheep (Ovis canadensis) to >50‐fold coverage to identify 2.8 million single nucleotide polymorphisms (SNPs) and genomic regions bearing signatures of directional selection (i.e. selective sweeps). A comparison of SNP diversity between the X chromosome and the autosomes indicated that bighorn males had a dramatically reduced long‐term effective population size compared to females. This probably reflects a long history of intense sexual selection mediated by male–male competition for mates. Selective sweep scans based on heterozygosity and nucleotide diversity revealed evidence for a selective sweep shared across multiple populations at RXFP2, a gene that strongly affects horn size in domestic ungulates. The massive horns carried by bighorn rams appear to have evolved in part via strong positive selection at RXFP2. We identified evidence for selection within individual populations at genes affecting early body growth and cellular response to hypoxia; however, these must be interpreted more cautiously as genetic drift is strong within local populations and may have caused false positives. These results represent a rare example of strong genomic signatures of selection identified at genes with known function in wild populations of a nonmodel species. Our results also showcase the value of reference genome assemblies from agricultural or model species for studies of the genomic basis of adaptation in closely related wild taxa.     

Genetic divergence of the Mesoamerican azure‐crowned hummingbird (Amazilia cyanocephala,Trochilidae) across the Motagua‐Polochic‐Jocotán fault system

The cloud forests of Mesoamerica are highly endangered habitats and the existence of narrowly distributed cryptic endemics will increase the number of taxa at potential risk of extinction. Here, we investigate genetic divergence between populations of the azure‐crowned hummingbird (Amazilia cyanocephala), a species complex of endemic hummingbirds to the montane forests of Mesoamerica, by analysing DNA sequences of four mitochondrial markers, morphological data and ecological niche modelling. Our results revealed the presence of two mtDNA lineages corresponding to subspecies A. c. cyanocephala distributed from Tamaulipas to Chiapas in Mexico and Amazilia c. guatemalensis distributed from southern Chiapas to Guatemala. The lineage split can be explained as a consequence of relative isolation of the populations in the different mountain ranges separated by the Motagua‐Polochic‐Jocotán fault system and corresponds to differences in morphology and to the lack of overlap in environmental space between subspecies. The divergence time estimates do not support the proposed model of a highly constrained temporal window at the end of the Pliocene as divergence at this barrier between cyanocephala and guatemalensis and splits of other bird taxa occurred during the Pleistocene.     

Exploring a Pool‐seq‐only approach for gaining population genomic insights in nonmodel species

Developing genomic insights is challenging in nonmodel species for which resources are often scarce and prohibitively costly. Here, we explore the potential of a recently established approach using Pool‐seq data to generate a de novo genome assembly for mining exons, upon which Pool‐seq data are used to estimate population divergence and diversity. We do this for two pairs of sympatric populations of brown trout (Salmo trutta): one naturally sympatric set of populations and another pair of populations introduced to a common environment. We validate our approach by comparing the results to those from markers previously used to describe the populations (allozymes and individual‐based single nucleotide polymorphisms [SNPs]) and from mapping the Pool‐seq data to a reference genome of the closely related Atlantic salmon (Salmo salar). We find that genomic differentiation (F_ST) between the two introduced populations exceeds that of the naturally sympatric populations (F_ST = 0.13 and 0.03 between the introduced and the naturally sympatric populations, respectively), in concordance with estimates from the previously used SNPs. The same level of population divergence is found for the two genome assemblies, but estimates of average nucleotide diversity differ ( ≈ 0.002 and  ≈ 0.001 when mapping to S. trutta and S. salar, respectively), although the relationships between population values are largely consistent. This discrepancy might be attributed to biases when mapping to a haploid condensed assembly made of highly fragmented read data compared to using a high‐quality reference assembly from a divergent species. We conclude that the Pool‐seq‐only approach can be suitable for detecting and quantifying genome‐wide population differentiation, and for comparing genomic diversity in populations of nonmodel species where reference genomes are lacking.     

Genome assembly and annotation of a Drosophila simulans strain from Madagascar

Drosophila simulans is a close relative of the genetic model D. melanogaster. Its worldwide distribution in combination with the absence of segregating chromosomal inversions makes this species an increasingly attractive model to study the molecular signatures of adaptation in natural and experimental populations. In an effort to improve the genomic resources for D. simulans, we assembled and annotated the genome of a strain originating from Madagascar (M252), the ancestral range of D. simulans. The comparison of the M252 genome to other available D. simulans assemblies confirmed its high quality, but also highlighted genomic regions that are difficult to assemble with NGS data. The annotation of M252 provides a clear improvement with alternative splicing for 52% of the multiple‐exon genes, UTRs for 70% of the genes, 225 novel genes and 781 pseudogenes being reported. We anticipate that the M252 genome will be a valuable resource for many research questions.     

Haplotype‐based genotyping‐by‐sequencing in oat genome research

In a de novo genotyping‐by‐sequencing (GBS) analysis of short, 64‐base tag‐level haplotypes in 4657 accessions of cultivated oat, we discovered 164741 tag‐level (TL) genetic variants containing 241224 SNPs. From this, the marker density of an oat consensus map was increased by the addition of more than 70000 loci. The mapped TL genotypes of a 635‐line diversity panel were used to infer chromosome‐level (CL) haplotype maps. These maps revealed differences in the number and size of haplotype blocks, as well as differences in haplotype diversity between chromosomes and subsets of the diversity panel. We then explored potential benefits of SNP vs. TL vs. CL GBS variants for mapping, high‐resolution genome analysis and genomic selection in oats. A combined genome‐wide association study (GWAS) of heading date from multiple locations using both TL haplotypes and individual SNP markers identified 184 significant associations. A comparative GWAS using TL haplotypes, CL haplotype blocks and their combinations demonstrated the superiority of using TL haplotype markers. Using a principal component‐based genome‐wide scan, genomic regions containing signatures of selection were identified. These regions may contain genes that are responsible for the local adaptation of oats to Northern American conditions. Genomic selection for heading date using TL haplotypes or SNP markers gave comparable and promising prediction accuracies of up to r = 0.74. Genomic selection carried out in an independent calibration and test population for heading date gave promising prediction accuracies that ranged between r = 0.42 and 0.67. In conclusion, TL haplotype GBS‐derived markers facilitate genome analysis and genomic selection in oat.     

Population genomic analysis uncovers African and European admixture in Drosophila melanogaster populations from the south‐eastern United States and Caribbean Islands

Drosophila melanogaster is postulated to have colonized North America in the past several 100 years in two waves. Flies from Europe colonized the east coast United States while flies from Africa inhabited the Caribbean, which if true, make the south‐east US and Caribbean Islands a secondary contact zone for African and European D. melanogaster. This scenario has been proposed based on phenotypes and limited genetic data. In our study, we have sequenced individual whole genomes of flies from populations in the south‐east US and Caribbean Islands and examined these populations in conjunction with population sequences from the west coast US, Africa, and Europe. We find that west coast US populations are closely related to the European population, likely reflecting a rapid westward expansion upon first settlements into North America. We also find genomic evidence of African and European admixture in south‐east US and Caribbean populations, with a clinal pattern of decreasing proportions of African ancestry with higher latitude. Our genomic analysis of D. melanogaster populations from the south‐east US and Caribbean Islands provides more evidence for the Caribbean Islands as the source of previously reported novel African alleles found in other east coast US populations. We also find the border between the south‐east US and the Caribbean island to be the admixture hot zone where distinctly African‐like Caribbean flies become genomically more similar to European‐like south‐east US flies. Our findings have important implications for previous studies examining the generation of east coast US clines via selection.     

Genome‐scale sampling suggests cryptic epigenetic structuring and insular divergence in Canada lynx

Determining the molecular signatures of adaptive differentiation is a fundamental component of evolutionary biology. A key challenge is to identify such signatures in wild organisms, particularly between populations of highly mobile species that undergo substantial gene flow. The Canada lynx (Lynx canadensis) is one species where mainland populations appear largely undifferentiated at traditional genetic markers, despite inhabiting diverse environments and displaying phenotypic variation. Here, we used high‐throughput sequencing to investigate both neutral genetic structure and epigenetic differentiation across the distributional range of Canada lynx. Newfoundland lynx were identified as the most differentiated population at neutral genetic markers, with demographic modelling suggesting that divergence from the mainland occurred at the end of the last glaciation (20–33 KYA). In contrast, epigenetic structure revealed hidden levels of differentiation across the range coincident with environmental determinants including winter conditions, particularly in the peripheral Newfoundland and Alaskan populations. Several biological pathways related to morphology were differentially methylated between populations, suggesting that epigenetic modifications might explain morphological differences seen between geographically peripheral populations. Our results indicate that epigenetic modifications, specifically DNA methylation, are powerful markers to investigate population differentiation in wild and non‐model systems.     

Hybridization in natural sympatric populations of Dermacentor ticks in northwestern North America

Hybridization in ticks has been described in a handful of species and mostly as a result of laboratory experiments. We used 148 AFLP loci to describe putative hybridization events between D. andersoni and D. variabilis in sympatric populations from northwestern North America. Recently, D. variabilis has expanded its range westward into the natural range of D. andersoni. Using a sample of 235 D. andersoni and 62 D. variabilis, we identified 31 individuals as putative hybrids: four F₂ individuals and 27 backcrosses to D. andersoni (as defined by NewHybrids ). We found no evidence of hybrids backcrossing into D. variabilis. Furthermore, all hybrids presented 16S mtDNA signatures characteristic of D. andersoni, which indicates the directionality of the hybrid crosses: female D. andersoni × male D. variabilis. We also discovered 13 species‐specific AFLP fragments for D. andersoni. These loci were found to have a decreased occurrence in the putative hybrids and were absent altogether in D. variabilis samples. AFLP profiles were also used to determine the levels of genetic population structure and gene flow among nine populations of D. andersoni and three of D. variabilis. Genetic structure exists in both species (D. andersoni, Φ_ST = 0.110; D. variabilis, Φ_ST = 0.304) as well as significant estimates of isolation by distance (D. andersoni, ρ = 0.066, P = 0.001; D. variabilis, ρ = 0.729, P = 0.001).     

Population structure and gene flow in the global pest,Helicoverpa armigera

Helicoverpa armigera is a major agricultural pest that is distributed across Europe, Asia, Africa and Australasia. This species is hypothesized to have spread to the Americas 1.5 million years ago, founding a population that is at present, a distinct species, Helicoverpa zea. In 2013, H. armigera was confirmed to have re‐entered South America via Brazil and subsequently spread. The source of the recent incursion is unknown and population structure in H. armigera is poorly resolved, but a basic understanding would highlight potential biosecurity failures and determine the recent evolutionary history of region‐specific lineages. Here, we integrate several end points derived from high‐throughput sequencing to assess gene flow in H. armigera and H. zea from populations across six continents. We first assemble mitochondrial genomes to demonstrate the phylogenetic relationship of H. armigera with other Heliothine species and the lack of distinction between populations. We subsequently use de novo genotyping‐by‐sequencing and whole‐genome sequences aligned to bacterial artificial chromosomes, to assess levels of admixture. Primarily, we find that Brazilian H. armigera are derived from diverse source populations, with strong signals of gene flow from European populations, as well as prevalent signals of Asian and African ancestry. We also demonstrate a potential field‐caught hybrid between H. armigera and H. zea, and are able to provide genomic support for the presence of the H. armigera conferta subspecies in Australasia. While structure among the bulk of populations remains unresolved, we present distinctions that are pertinent to future investigations as well as to the biosecurity threat posed by H. armigera.     

Characterization of a Y‐specific duplication/insertion of the anti‐Mullerian hormone type II receptor gene based on a chromosome‐scale genome assembly of yellow perch,Perca flavescens

Yellow perch, Perca flavescens, is an ecologically and economically important species native to a large portion of the northern United States and southern Canada and is also a promising candidate species for aquaculture. However, no yellow perch reference genome has been available to facilitate improvements in both fisheries and aquaculture management practices. By combining Oxford Nanopore Technologies long‐reads, 10X Genomics Illumina short linked reads and a chromosome contact map produced with Hi‐C, we generated a high‐continuity chromosome‐scale yellow perch genome assembly of 877.4 Mb. It contains, in agreement with the known diploid chromosome yellow perch count, 24 chromosome‐size scaffolds covering 98.8% of the complete assembly (N50 = 37.4 Mb, L50 = 11). We also provide a first characterization of the yellow perch sex determination locus that contains a male‐specific duplicate of the anti‐Mullerian hormone type II receptor gene (amhr2by) inserted at the proximal end of the Y chromosome (chromosome 9). Using this sex‐specific information, we developed a simple PCR genotyping assay which accurately differentiates XY genetic males (amhr2by⁺) from XX genetic females (amhr2by^?). Our high‐quality genome assembly is an important genomic resource for future studies on yellow perch ecology, toxicology, fisheries and aquaculture research. In addition, characterization of the amhr2by gene as a candidate sex‐determining gene in yellow perch provides a new example of the recurrent implication of the transforming growth factor beta pathway in fish sex determination, and highlights gene duplication as an important genomic mechanism for the emergence of new master sex determination genes.