Patterns Of Genomic Divergence Research Articles

First chromosome scale genomes of ithomiine butterflies (Nymphalidae: Ithomiini): Comparative models for mimicry genetic studies.

The ithomiine butterflies (Nymphalidae: Danainae) represent the largest known radiation of Müllerian mimetic butterflies. They dominate by number the mimetic butterfly communities, which include species such as the iconic neotropical Heliconius genus. Recent studies on the ecology and genetics of speciation in Ithomiini have suggested that sexual pheromones, colour pattern and perhaps hostplant could drive reproductive isolation. However, no reference genome was available for Ithomiini, which has hindered further exploration on the genetic architecture of these candidate traits, and more generally on the genomic patterns of divergence. Here, we generated high-quality, chromosome-scale genome assemblies for two Melinaea species, M. marsaeus and M. menophilus, and a draft genome of the species Ithomia salapia. We obtained genomes with a size ranging from 396 to 503 Mb across the three species and scaffold N50 of 40.5 and 23.2Mb for the two chromosome-scale assemblies. Using collinearity analyses we identified massive rearrangements between the two closely related Melinaea species. An annotation of transposable elements and gene content was performed, as well as a specialist annotation to target chemosensory genes, which is crucial for host plant detection and mate recognition in mimetic species. A comparative genomic approach revealed independent gene expansions in ithomiines and particularly in gustatory receptor genes. These first three genomes of ithomiine mimetic butterflies constitute a valuable addition and a welcome comparison to existing biological models such as Heliconius, and will enable further understanding of the mechanisms of adaptation in butterflies.

Genomic Diversity and Evolution of Quasispecies in Newcastle Disease Virus Infections.

Newcastle disease virus (NDV) infections are well known to harbour quasispecies, due to the error-prone nature of the RNA polymerase. Quasispecies variants in the fusion cleavage site of the virus are known to significantly change its virulence. However, little is known about the genomic patterns of diversity and selection in NDV viral swarms. We analyse deep sequencing data from in vitro and in vivo NDV infections to uncover the genomic patterns of diversity and the signatures of selection within NDV swarms. Variants in viruses from in vitro samples are mostly localised in non-coding regions and 3′ and 5′ untranslated regions (3′UTRs or 5′UTRs), while in vivo samples contain an order of magnitude more variants. We find different patterns of genomic divergence and diversity among NDV genotypes, as well as differences in the genomic distribution of intra-host variants among in vitro and in vivo infections of the same strain. The frequency spectrum shows clear signatures of intra-host purifying selection in vivo on the matrix protein (M) coding gene and positive or diversifying selection on nucleocapsid (NP) and haemagglutinin-neuraminidase (HN). The comparison between within-host polymorphisms and phylogenetic divergence reveals complex patterns of selective pressure on the NDV genome at between- and within-host level. The M sequence is strongly constrained both between and within hosts, fusion protein (F) coding gene is under intra-host positive selection, and NP and HN show contrasting patterns: HN RNA sequence is positively selected between hosts while its protein sequence is positively selected within hosts, and NP is under intra-host positive selection at the RNA level and negative selection at the protein level.

Genome-wide patterns of divergence and introgression after secondary contact between Pungitius sticklebacks.

Speciation is a continuous process. Although it is known that differential adaptation can initiate divergence even in the face of gene flow, we know relatively little about the mechanisms driving complete reproductive isolation and the genomic patterns of divergence and introgression at the later stages of speciation. Sticklebacks contain many pairs of sympatric species differing in levels of reproductive isolation and divergence history. Nevertheless, most previous studies have focused on young species pairs. Here, we investigated two sympatric stickleback species, Pungitius pungitius and P. sinensis, whose habitats overlap in eastern Hokkaido; these species show hybrid male sterility, suggesting that they may be at a late stage of speciation. Our demographic analysis using whole-genome sequence data showed that these species split 1.73 Ma and came into secondary contact 37 200 years ago after a period of allopatry. This long period of allopatry might have promoted the evolution of intrinsic incompatibility. Although we detected on-going gene flow and signatures of introgression, overall genomic divergence was high, with considerable heterogeneity across the genome. The heterogeneity was significantly associated with variation in recombination rate. This sympatric pair provides new avenues to investigate the late stages of the stickleback speciation continuum. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Patterns of Genomic Divergence and Signals of Selection in Sympatric and Allopatric Northeastern Pacific and Sea of Cortez Populations of the Sargo (Anisotremus davidsonii) and Longjaw Mudsucker (Gillichthys mirabilis).

Studying how isolation can impact population divergence and adaptation in co-distributed species can bring us closer to understanding how landscapes affect biodiversity. The Sargo, Anisotremus davidsonii (Haemulidae), and the Longjaw mudsucker, Gillichthys mirabilis (Gobiidae), offer a notable framework to study such mechanisms as their Pacific populations cross phylogeographic breaks at Point Conception, California, United States, and Punta Eugenia, Mexico, and are separated to those in the Sea of Cortez by the Baja California peninsula. Here, thousands of loci are genotyped from 48 Sargos and 73 mudsuckers using RADseq to characterize overall genomic divergence, and search for common patterns of putatively neutral and non-neutral structure based on outlier loci among populations with hypothesized different levels of isolation. We further search for parallels between population divergence and the total proportion of outliers, outlier FST distribution, and the proportion of outliers matching coding regions in GenBank. Statistically significant differentiation is seen across Point Conception in mudsucker (FST = 0.15), Punta Eugenia in Sargo (FST = 0.02), and on either side of the Baja California peninsula in both species (FST = 0.11 and 0.23, in Sargo and mudsucker, respectively). Each species shows structure using neutral and non-neutral loci. Finally, higher population divergence yields a more even distribution of outliers along their differentiation range but does not always translate into higher outlier proportions or higher rates in which outliers are matched to coding regions. If repeated in similar systems, observed genomic patterns might reveal speciation signatures in diverse networks of population isolation.

How predictable is genome evolution?

Similar patterns of genomic divergence have been observed in the evolution of plant species separated by oceans.

Divergence with gene flow is driven by local adaptation to temperature and soil phosphorus concentration in teosinte subspecies (Zea mays parviglumis and Zea mays mexicana).

Patterns of genomic divergence between hybridizing taxa can be heterogeneous along the genome. Both differential introgression and local adaptation may contribute to this pattern. Here, we analysed two teosinte subspecies, Zea mays ssp. parviglumis and ssp. mexicana, to test whether their divergence has occurred in the face of gene flow and to infer which environmental variables have been important drivers of their ecological differentiation. We generated 9,780 DArTseqTM SNPs for 47 populations, and used an additional data set containing 33,454 MaizeSNP50 SNPs for 49 populations. With these data, we inferred features of demographic history and performed genome wide scans to determine the number of outlier SNPs associated with climate and soil variables. The two data sets indicate that divergence has occurred or been maintained despite continuous gene flow and/or secondary contact. Most of the significant SNP associations were to temperature and to phosphorus concentration in the soil. A large proportion of these candidate SNPs were located in regions of high differentiation that had been identified previously as putative inversions. We therefore propose that genomic differentiation in teosintes has occurred by a process of adaptive divergence, with putative inversions contributing to reduced gene flow between locally adapted populations.

Analysis of Genome-Wide Differentiation between Native and Introduced Populations of the Cupped Oysters Crassostrea gigas and Crassostrea angulata.

The Pacific cupped oyster is genetically subdivided into two sister taxa, Crassostrea gigas and Crassostrea angulata, which are in contact in the north-western Pacific. The nature and origin of their genetic and taxonomic differentiation remains controversial due the lack of known reproductive barriers and the high degree of morphologic similarity. In particular, whether the presence of ecological and/or intrinsic isolating mechanisms contributes to species divergence is unknown. The recent co-introduction of both taxa into Europe offers a unique opportunity to test how genetic differentiation is maintained under new environmental and demographic conditions. We generated a pseudochromosome assembly of the Pacific oyster genome using a combination of BAC-end sequencing and scaffold anchoring to a new high-density linkage map. We characterized genome-wide differentiation between C. angulata and C. gigas in both their native and introduced ranges, and showed that gene flow between species has been facilitated by their recent co-introductions in Europe. Nevertheless, patterns of genomic divergence between species remain highly similar in Asia and Europe, suggesting that the environmental transition caused by the co-introduction of the two species did not affect the genomic architecture of their partial reproductive isolation. Increased genetic differentiation was preferentially found in regions of low recombination. Using historical demographic inference, we show that the heterogeneity of differentiation across the genome is well explained by a scenario whereby recent gene flow has eroded past differentiation at different rates across the genome after a period of geographical isolation. Our results thus support the view that low-recombining regions help in maintaining intrinsic genetic differences between the two species.

Effects of assortative mate choice on the genomic and morphological structure of a hybrid zone between two bird subspecies.

Phenotypic differentiation plays an important role in the formation and maintenance of reproductive barriers. In some cases, variation in a few key aspects of phenotype can promote and maintain divergence; hence, the identification of these traits and their associations with patterns of genomic divergence is crucial for understanding the patterns and processes of population differentiation. We studied hybridization between the alba and personata subspecies of the white wagtail (Motacilla alba), and quantified divergence and introgression of multiple morphological traits and 19,437 SNP loci on a 3,000km transect. Our goal was to identify traits that may contribute to reproductive barriers and to assess how variation in these traits corresponds to patterns of genome-wide divergence. Variation in only one trait-head plumage patterning-was consistent with reproductive isolation. Transitions in head plumage were steep and occurred over otherwise morphologically and genetically homogeneous populations, whereas cline centres for other traits and genomic ancestry were displaced over 100km from the head cline. Field observational data show that social pairs mated assortatively by head plumage, suggesting that these phenotypes are maintained by divergent mating preferences. In contrast, variation in all other traits and genetic markers could be explained by neutral diffusion, although weak ecological selection cannot be ruled out. Our results emphasize that assortative mating may maintain phenotypic differences independent of other processes shaping genome-wide variation, consistent with other recent findings that raise questions about the relative importance of mate choice, ecological selection and selectively neutral processes for divergent evolution.

Genomic adaptation to agricultural environments: cabbage white butterflies (Pieris rapae) as a case study

BackgroundAgricultural environments have long presented an opportunity to study evolution in action, and genomic approaches are opening doors for testing hypotheses about adaptation to crops, pesticides, and fertilizers. Here, we begin to develop the cabbage white butterfly (Pieris rapae) as a system to test questions about adaptation to novel, agricultural environments. We focus on a population in the north central United States as a unique case study: here, canola, a host plant, has been grown during the entire flight period of the butterfly over the last three decades.ResultsFirst, we show that the agricultural population has diverged phenotypically relative to a nonagricultural population: when reared on a host plant distantly related to canola, the agricultural population is smaller and more likely to go into diapause than the nonagricultural population. Second, drawing from deep sequencing runs from six individuals from the agricultural population, we assembled the gut transcriptome of this population. Then, we sequenced RNA transcripts from the midguts of 96 individuals from this canola agricultural population and the nonagricultural population in order to describe patterns of genomic divergence between the two. While population divergence is low, 235 genes show evidence of significant differentiation between populations. These genes are significantly enriched for cofactor and small molecule metabolic processes, and many genes also have transporter or catalytic activity. Analyses of population structure suggest the agricultural population contains a subset of the genetic variation in the nonagricultural population.ConclusionsTaken together, our results suggest that adaptation of cabbage whites to an agricultural environment occurred at least in part through selection on standing genetic variation. Both the phenotypic and genetic data are consistent with the idea that this pest has adapted to an abundant and predictable agricultural resource through a narrowing of niche breadth and loss of genetic variants rather than de novo gain of adaptive alleles. The present research develops genomic resources to pave the way for future studies using cabbage whites as a model contributing to our understanding of adaptation to agricultural environments.

Insight into the roles of selection in speciation from genomic patterns of divergence and introgression in secondary contact in venomous rattlesnakes.

Investigating secondary contact of historically isolated lineages can provide insight into how selection and drift influence genomic divergence and admixture. Here, we studied the genomic landscape of divergence and introgression following secondary contact between lineages of the Western Diamondback Rattlesnake (Crotalus atrox) to determine whether genomic regions under selection in allopatry also contribute to reproductive isolation during introgression. We used thousands of nuclear loci to study genomic differentiation between two lineages that have experienced recent secondary contact following isolation, and incorporated sampling from a zone of secondary contact to identify loci that are resistant to gene flow in hybrids. Comparisons of patterns of divergence and introgression revealed a positive relationship between allelic differentiation and resistance to introgression across the genome, and greater‐than‐expected overlap between genes linked to lineage‐specific divergence and loci that resist introgression. Genes linked to putatively selected markers were related to prominent aspects of rattlesnake biology that differ between populations of Western Diamondback rattlesnakes (i.e., venom and reproductive phenotypes). We also found evidence for selection against introgression of genes that may contribute to cytonuclear incompatibility, consistent with previously observed biased patterns of nuclear and mitochondrial alleles suggestive of partial reproductive isolation due to cytonuclear incompatibilities. Our results provide a genome‐scale perspective on the relationships between divergence and introgression in secondary contact that is relevant for understanding the roles of selection in maintaining partial isolation of lineages, causing admixing lineages to not completely homogenize.

Investigating genomic and phenotypic parallelism between piscivorous and planktivorous lake trout (Salvelinus namaycush) ecotypes by means of RADseq and morphometrics analyses.

Repeated adaptive ecological diversification has commonly been reported in fish and has often been associated with trophic niche diversity. The main goal of this study was to investigate the extent of parallelism in the genomic and phenotypic divergence between piscivorous and planktivorous lake trout ecotypes from Laurentian Shield lakes, Canada. This was achieved by documenting the extent of morphological differentiation using geometric morphometrics and linear measurements as well as the pattern of genomic divergence by means of RADseq genotyping (3925 filtered SNPs) in 12 lakes. Our results indicate that the two ecotypes evolved distinct body shape and several linear measurements in parallel. Neutral genetic differentiation was pronounced between all isolated populations (Mean FST =0.433), indicating no or very limited migration and pronounced genetic drift. Significant genetic differentiation also suggested partial reproductive isolation between ecotypes in the two lakes where they are found in sympatry. Combining different outlier detection methods, we identified 48 SNPs putatively under divergent selection between ecotypes, among which 10 could be annotated and related to functions such as developmental processes and ionic regulation. Finally, our results indicate that parallel morphological divergence is accompanied by both parallel and nonparallel genomic divergence, which is associated with the use of different trophic niches between ecotypes. The results are also discussed in the context of management and conservation of this highly exploited species throughout northern North America.

History repeats itself: genomic divergence in copepods.

Press stop, erase everything from now till some arbitrary time in the past and start recording life as it evolves once again. Would you see the same tape of life playing itself over and over, or would a different story unfold every time? The late Steven Jay Gould called this experiment replaying the tape of life and argued that any replay of the tape would lead evolution down a pathway radically different from the road actually taken (Gould 1989). This thought experiment has puzzled evolutionary biologists for a long time: how repeatable are evolutionary events? And if history does indeed repeat itself, what are the factors that may help us predict the path taken? A powerful means to address these questions at a small evolutionary scale is to study closely related populations that have evolved independently, under similar environmental conditions. This is precisely what Pereira et al. (2016) set out to do using marine copepods Tigriopus californicus, and present their results in this issue of Molecular Ecology. They show that evolution can be repeatable and even partly predictable, at least at the molecular level. As expected from theory, patterns of divergence were shaped by natural selection. At the same time, strong genetic drift due to small population sizes also constrained evolution down a similar evolutionary road, and probably contributed to repeatable patterns of genomic divergence.

Distinguishing noise from signal in patterns of genomic divergence in a highly polymorphic avian radiation.

Recently diverged taxa provide the opportunity to search for the genetic basis of the phenotypes that distinguish them. Genomic scans aim to identify loci that are diverged with respect to an otherwise weakly differentiated genetic background. These loci are candidates for being past targets of selection because they behave differently from the rest of the genome that has either not yet differentiated or that may cross species barriers through introgressive hybridization. Here we use a reduced-representation genomic approach to explore divergence among six species of southern capuchino seedeaters, a group of recently radiated sympatric passerine birds in the genus Sporophila. For the first time in these taxa, we discovered a small proportion of markers that appeared differentiated among species. However, when assessing the significance of these signatures of divergence, we found that similar patterns can also be recovered from random grouping of individuals representing different species. A detailed demographic inference indicates that genetic differences among Sporophila species could be the consequence of neutral processes, which include a very large ancestral effective population size that accentuates the effects of incomplete lineage sorting. As these neutral phenomena can generate genomic scan patterns that mimic those of markers involved in speciation and phenotypic differentiation, they highlight the need for caution when ascertaining and interpreting differentiated markers between species, especially when large numbers of markers are surveyed. Our study provides new insights into the demography of the southern capuchino radiation and proposes controls to distinguish signal from noise in similar genomic scans.

Genomics of divergence along a continuum of parapatric population differentiation.

The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.

Strategies to Identify Adaptive Genes in Hybridizing Trees like Oaks and Poplars

Ecologically divergent, hybridizing species such as oaks and poplars provide models to identify genomic regions under selection and adaptive alleles that are transferred between species in hybrid zones. Oaks show patterns of genomic divergence characteristic for early stages of speciation with gene flow, in which large genomic regions are homogenized by interspecific gene flow interspersed by smaller regions (outlier regions) with high interspecific differentiation as result of divergent selection. These outlier regions can be identified using genome scans in hybrid zones and anchored to the Quercus robur genome sequence which will become available in the near future. Combined outlier and association genetic approaches can assess the role of individual genes in outlier genomic regions in adaptive trait variation. In contrast, hybridizing poplar species show a pattern of genomic divergence with large genomic regions of high interspecific differentiation punctuated by smaller regions of low differentiation as the result of interspecific gene flow. Genome scans in multiple hybrid zones of interfertile poplar species and in populations outside the area of sympatry will allow for the identification of genes that are exchanged between species by interspecific gene flow using the Populus trichocarpa genome sequence as a reference. Again association genetic approaches can be used for the characterization of variation in these introgressed genes with adaptive trait variation. In the present paper, the application of genomic approaches to identify genes for adaptive species divergence and reproductive isolation, and introgressed genes between species is discussed.

High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species.

Hybridization is increasingly being recognized as a common process in both animal and plant species. Negative epistatic interactions between genes from different parental genomes decrease the fitness of hybrids and can limit gene flow between species. However, little is known about the number and genome-wide distribution of genetic incompatibilities separating species. To detect interacting genes, we perform a high-resolution genome scan for linkage disequilibrium between unlinked genomic regions in naturally occurring hybrid populations of swordtail fish. We estimate that hundreds of pairs of genomic regions contribute to reproductive isolation between these species, despite them being recently diverged. Many of these incompatibilities are likely the result of natural or sexual selection on hybrids, since intrinsic isolation is known to be weak. Patterns of genomic divergence at these regions imply that genetic incompatibilities play a significant role in limiting gene flow even in young species.