Genome Speciation Research Articles

Linked Selection and Gene Density Shape Genome-Wide Patterns of Diversification in Peatmosses.

Genome evolution under speciation is poorly understood in nonmodel and nonvascular plants, such as bryophytes-the largest group of nonvascular land plants. Their genomes are structurally different from angiosperms and likely subjected to stronger linked selection pressure, which may have profound consequences on genome evolution in diversifying lineages, even more so when their genome architecture is conserved. We use the highly diverse, rapidly radiated group of peatmosses (Sphagnum) to characterize the processes affecting genome diversification in bryophytes. Using whole-genome sequencing data from populations of 12 species sampled at different phylogenetic and geographical scales, we describe high correlation of the genomic landscapes of differentiation, divergence, and diversity in Sphagnum. Coupled with evidence from the patterns of covariation among different measures of genetic diversity, phylogenetic discordance, and gene density, this provides strong support that peatmoss genome evolution has been shaped by the long-term effects of linked selection, constrained by distribution of selection targets in the genome. Thus, peatmosses join the growing number of animal and plant groups where functional features of the genome, such as gene density, and linked selection drive genome evolution along predetermined and highly similar routes in different species. Our findings demonstrate the great potential of bryophytes for studying the genomics of speciation and highlight the urgent need to expand the genomic resources in this remarkable group of plants.

A three-dimensional genomics view for speciation research

Genomic information is folded in a three-dimensional (3D) structure, a rarely explored evolutionary driver of speciation. Technological advances now enable the study of 3D genome structures (3DGSs) across the Tree of Life. At the onset of 3D speciation genomics, we discuss the putative roles of 3DGSs in speciation.

Linked selection and recombination rate generate both shared and lineage‐specific genomic islands of divergence in two independent Quercus species pairs

AbstractA fundamental question in speciation genomics is how evolutionary processes shape the genomic landscape of differentiation between species. Regions of elevated differentiation, referred to as genomic islands, could be shared among closely related species (shared islands) or specific to a lineage (lineage‐specific islands). Shared islands are typically assumed to result from background selection. However, simulations and empirical studies have suggested that positive selection contributes to both shared and lineage‐specific islands. Here, we utilized comparative population genomics to examine the contributions of different evolutionary processes to patterns of genetic differentiation when gene flow and incomplete lineage sorting are minimal. We used whole‐genome resequencing data for 135 individuals from four oak species, including two independent species pairs, Quercus variabilis Blume and Quercus acutissima Carruth. in the subgenus Cerris, and Quercus dentata Thunb. and Quercus griffithii Hook.f. & Thomson ex Miq. in the subgenus Quercus. We found that both shared and subgenus‐specific islands were caused by positive selection, including selective sweeps in current populations and in their most recent common ancestors. Moreover, the recombination rate was a better predictor of genomic differentiation than gene density. Overall, our results reveal that recombination and positive selection impacted genomic differentiation considerably and provide a more precise grasp of how genomic islands formed in Quercus.

Insights into chloroplast genome structure and phylogenetic relationships within the Sesamum species complex (Pedaliaceae).

Background: In the Sesamum species complex, the lack of wild species genomic resources hinders the evolutionary comprehension of phylogenetic relationships. Results: In the present study, we generated complete chloroplast genomes of six wild relatives (Sesamum alatum, Sesamum angolense, Sesamum pedaloides, Ceratotheca sesamoides (syn. Sesamum sesamoides), Ceratotheca triloba (syn. Sesamum trilobum), and Sesamum radiatum) and a Korean cultivar, Sesamum indicum cv. Goenbaek. A typical quadripartite chloroplast structure, including two inverted repeats (IR), a large single copy (LSC), and a small single copy (SSC), was observed. A total of 114 unique genes encompassing 80 coding genes, four ribosomal RNAs, and 30 transfer RNAs were counted. The chloroplast genomes (152, 863-153, 338bp) exhibited the IR contraction/expansion phenomenon and were quite conserved in both coding and non-coding regions. However, high values of the nucleotide diversity index were found in several genes, including ndhA, ndhE, ndhF, ycf1, and psaC-ndhD. Concordant tree topologies suggest ndhF as a useful marker for taxon discrimination. The phylogenetic inference and time divergence dating indicate that S. radiatum (2n = 64) occurred concomitantly with the sister species C. sesamoides (2n = 32) approximately 0.05million years ago (Mya). In addition, S. alatum was clearly discriminated by forming a single clade, showing its long genetic distance and potential early speciation event in regards to the others. Conclusion: Altogether, we propose to rename C. sesamoides and C. triloba as S. sesamoides and S. trilobum, respectively, as suggested previously based on the morphological description. This study provides the first insight into the phylogenetic relationships among the cultivated and wild African native relatives. The chloroplast genome data lay a foundation for speciation genomics in the Sesamum species complex.

An annotated chromosome-scale reference genome for Eastern black-eared wheatear (Oenanthe melanoleuca).

Pervasive convergent evolution and in part high incidences of hybridization distinguish wheatears (songbirds of the genus Oenanthe) as a versatile system to address questions at the forefront of research on the molecular bases of phenotypic and species diversification. To prepare the genomic resources for this venture, we here generated and annotated a chromosome-scale assembly of the Eastern black-eared wheatear (Oenanthe melanoleuca). This species is part of the Oenanthe hispanica complex that is characterized by convergent evolution of plumage coloration and high rates of hybridization. The long-read-based male nuclear genome assembly comprises 1.04 Gb in 32 autosomes, the Z chromosome, and the mitogenome. The assembly is highly contiguous (contig N50, 12.6 Mb; scaffold N50, 70 Mb), with 96% of the genome assembled at the chromosome level and 95.5% benchmarking universal single-copy orthologs (BUSCO) completeness. The nuclear genome was annotated with 18,143 protein-coding genes and 31,333 mRNAs (annotation BUSCO completeness, 98.0%), and about 10% of the genome consists of repetitive DNA. The annotated chromosome-scale reference genome of Eastern black-eared wheatear provides a crucial resource for research into the genomics of adaptation and speciation in an intriguing group of passerines.

Chromosome fusions repatterned recombination rate and facilitated reproductive isolation during Pristionchus nematode speciation

Large-scale genome-structural evolution is common in various organisms. Recent developments in speciation genomics revealed the importance of inversions, whereas the role of other genome-structural rearrangements, including chromosome fusions, have not been well characterized. We study genomic divergence and reproductive isolation of closely related nematodes: the androdioecious (hermaphroditic) model Pristionchus pacificus and its dioecious sister species Pristionchus exspectatus. A chromosome-level genome assembly of P. exspectatus using single-molecule and Hi-C sequencing revealed a chromosome-wide rearrangement relative to P. pacificus. Strikingly, genomic characterization and cytogenetic studies including outgroup species Pristionchus occultus indicated two independent fusions involving the same chromosome, ChrIR, between these related species. Genetic linkage analysis indicated that these fusions altered the chromosome-wide pattern of recombination, resulting in large low-recombination regions that probably facilitated the coevolution between some of the ~14.8% of genes across the entire genomes. Quantitative trait locus analyses for hybrid sterility in all three sexes revealed that major quantitative trait loci mapped to the fused chromosome ChrIR. While abnormal chromosome segregations of the fused chromosome partially explain hybrid female sterility, hybrid-specific recombination that breaks linkage of genes in the low-recombination region was associated with hybrid male sterility. Thus, recent chromosome fusions repatterned recombination rate and drove reproductive isolation during Pristionchus speciation.

Heterogeneous Genomic Divergence Landscape in Two Commercially Important European Scallop Species.

Two commercially important scallop species of the genus Pecten are found in Europe: the north Atlantic Pecten maximus and the Mediterranean Pecten jacobaeus whose distributions abut at the Almeria-Orán front. Whilst previous studies have quantified genetic divergence between these species, the pattern of differentiation along the Pecten genome is unknown. Here, we mapped RADseq data from 235 P. maximus and 27 P. jacobaeus to a chromosome-level reference genome, finding a heterogeneous landscape of genomic differentiation. Highly divergent genomic regions were identified across 14 chromosomes, while the remaining five showed little differentiation. Demographic and comparative genomics analyses suggest that this pattern resulted from an initial extended period of isolation, which promoted divergence, followed by differential gene flow across the genome during secondary contact. Single nucleotide polymorphisms present within highly divergent genomic regions were located in areas of low recombination and contrasting patterns of LD decay were found between the two species, hinting at the presence of chromosomal inversions in P. jacobaeus. Functional annotations revealed that highly differentiated regions were enriched for immune-related processes and mRNA modification. While future work is necessary to characterize structural differences, this study provides new insights into the speciation genomics of P. maximus and P. jacobaeus.

Speciation genomics and the role of depth in the divergence of rockfishes (Sebastes) revealed through Pool-seq analysis of enriched sequences.

Speciation in the marine environment is challenged by the wide geographic distribution of many taxa and potential for high rates of gene flow through larval dispersal mechanisms. Depth has recently been proposed as a potential driver of ecological divergence in fishes, and yet it is unclear how adaptation along these gradients' shapes genomic divergence. The genus Sebastes contains numerous species pairs that are depth‐segregated and can provide a better understanding of the mode and tempo of genomic diversification. Here, we present exome data on two species pairs of rockfishes that are depth‐segregated and have different degrees of divergence: S. chlorostictus–S. rosenblatti and S. crocotulus–S. miniatus. We were able to reliably identify “islands of divergence” in the species pair with more recent divergence (S. chlorostictus–S. rosenblatti) and discovered a number of genes associated with neurosensory function, suggesting a role for this pathway in the early speciation process. We also reconstructed demographic histories of divergence and found the best supported model was isolation followed by asymmetric secondary contact for both species pairs. These results suggest past ecological/geographic isolation followed by asymmetric secondary contact of deep to shallow species. Our results provide another example of using rockfish as a model for studying speciation and support the role of depth as an important mechanism for diversification in the marine environment.

Whole-genome analysis of multiple wood ant population pairs supports similar speciation histories, but different degrees of gene flow, across their European ranges.

The application of demographic history modelling and inference to the study of divergence between species has become a cornerstone of speciation genomics. Speciation histories are usually reconstructed by analysing single populations from each species, assuming that the inferred population history represents the actual speciation history. However, this assumption may not be met when species diverge with gene flow, for example, when secondary contact may be confined to specific geographic regions. Here, we tested whether divergence histories inferred from heterospecific populations may vary depending on their geographic locations, using the two wood ant species Formica polyctena and F. aquilonia. We performed whole‐genome resequencing of 20 individuals sampled in multiple locations across the European ranges of both species. Then, we reconstructed the histories of distinct heterospecific population pairs using a coalescent‐based approach. Our analyses always supported a scenario of divergence with gene flow, suggesting that divergence started in the Pleistocene (c. 500 kya) and occurred with continuous asymmetrical gene flow from F. aquilonia to F. polyctena until a recent time, when migration became negligible (2–19 kya). However, we found support for contemporary gene flow in a sympatric pair from Finland, where the species hybridise, but no signature of recent bidirectional gene flow elsewhere. Overall, our results suggest that divergence histories reconstructed from a few individuals may be applicable at the species level. Nonetheless, the geographical context of populations chosen to represent their species should be taken into account, as it may affect estimates of migration rates between species when gene flow is spatially heterogeneous.

Genome assembly, structural variants, and genetic differentiation between lake whitefish young species pairs (Coregonus sp.) with long and short reads.

Nascent pairs of ecologically differentiated species offer an opportunity to get a better glimpse at the genetic architecture of speciation. Of particular interest is our recent ability to consider a wider range of genomic variants, not only single-nucleotide polymorphisms (SNPs), thanks to long-read sequencing technology. We can now identify structural variants (SVs) such as insertions, deletions and other rearrangements, allowing further insights into the genetic architecture of speciation and how different types of variants are involved in species differentiation. Here, we investigated genomic patterns of differentiation between sympatric species pairs (Dwarf and Normal) belonging to the lake whitefish (Coregonus clupeaformis) species complex. We assembled the first reference genomes for both C. clupeaformis sp. Normal and C. clupeaformis sp. Dwarf, annotated the transposable elements and analysed the genomes in the light of related coregonid species. Next, we used a combination of long- and short-read sequencing to characterize SVs and genotype them at the population scale using genome-graph approaches, showing that SVs cover five times more of the genome than SNPs. We then integrated both SNPs and SVs to investigate the genetic architecture of species differentiation in two different lakes and highlighted an excess of shared outliers of differentiation. In particular, a large fraction of SVs differentiating the two species correspond to insertions or deletions of transposable elements (TEs), suggesting that TE accumulation may represent a key component of genetic divergence between the Dwarf and Normal species. Together, our results suggest that SVs may play an important role in speciation and that, by combining second- and third-generation sequencing, we now have the ability to integrate SVs into speciation genomics.

Comparative Population Genomics of Cryptic Speciation and Adaptive Divergence in Bicknell's and Gray-Cheeked Thrushes (Aves: Catharus bicknelli and Catharus minimus).

Cryptic speciation may occur when reproductive isolation is recent or the accumulation of morphological differences between sister lineages is slowed by stabilizing selection preventing phenotypic differentiation. In North America, Bicknell’s Thrush (Catharus bicknelli) and its sister species, the Gray-cheeked Thrush (Catharus minimus), are parapatrically breeding migratory songbirds, distinguishable in nature only by subtle differences in song and coloration, and were recognized as distinct species only in the 1990s. Previous molecular studies have estimated that the species diverged approximately 120,000–420,000 YBP and found very low levels of introgression despite their similarity and sympatry in the spring (prebreeding) migration. To further clarify the history, genetic divergence, genomic structure, and adaptive processes in C. bicknelli and C. minimus, we sequenced and assembled high-coverage reference genomes of both species and resequenced genomes from population samples of C. bicknelli, C. minimus, and two individuals of the Swainson’s Thrush (Catharus ustulatus). The genome of C. bicknelli exhibits markedly higher abundances of transposable elements compared with other Catharus and chicken. Demographic and admixture analyses confirm moderate genome-wide differentiation (Fst 0.10) and limited gene flow between C. bicknelli and C. minimus, but suggest a more recent divergence than estimates based on mtDNA. We find evidence of rapid evolution of the Z-chromosome and elevated divergence consistent with natural selection on genomic regions near genes involved with neuronal processes in C. bicknelli. These genomes are a useful resource for future investigations of speciation, migration, and adaptation in Catharus thrushes.

Evolutionary case study: the genomics of speciation in Heliconius butterflies

Evolutionary case study: the genomics of speciation in Heliconius butterflies

DILS: Demographic inferences with linked selection by using ABC.

We present DILS, a deployable statistical analysis platform for conducting demographic inferences with linked selection from population genomic data using an Approximate Bayesian Computation framework. DILS takes as input single-population or two-population data sets (multilocus fasta sequences) and performs three types of analyses in a hierarchical manner, identifying: (a) the best demographic model to study the importance of gene flow and population size change on the genetic patterns of polymorphism and divergence, (b) the best genomic model to determine whether the effective size Ne and migration rate N, m are heterogeneously distributed along the genome (implying linked selection) and (c) loci in genomic regions most associated with barriers to gene flow. Also available via a Web interface, an objective of DILS is to facilitate collaborative research in speciation genomics. Here, we show the performance and limitations of DILS by using simulations and finally apply the method to published data on a divergence continuum composed by 28 pairs of Mytilus mussel populations/species.

Tectonics, climate and the diversification of the tropical African terrestrial flora and fauna.

ABSTRACTTropical Africa is home to an astonishing biodiversity occurring in a variety of ecosystems. Past climatic change and geological events have impacted the evolution and diversification of this biodiversity. During the last two decades, around 90 dated molecular phylogenies of different clades across animals and plants have been published leading to an increased understanding of the diversification and speciation processes generating tropical African biodiversity. In parallel, extended geological and palaeoclimatic records together with detailed numerical simulations have refined our understanding of past geological and climatic changes in Africa. To date, these important advances have not been reviewed within a common framework. Here, we critically review and synthesize African climate, tectonics and terrestrial biodiversity evolution throughout the Cenozoic to the mid‐Pleistocene, drawing on recent advances in Earth and life sciences. We first review six major geo‐climatic periods defining tropical African biodiversity diversification by synthesizing 89 dated molecular phylogeny studies. Two major geo‐climatic factors impacting the diversification of the sub‐Saharan biota are highlighted. First, Africa underwent numerous climatic fluctuations at ancient and more recent timescales, with tectonic, greenhouse gas, and orbital forcing stimulating diversification. Second, increased aridification since the Late Eocene led to important extinction events, but also provided unique diversification opportunities shaping the current tropical African biodiversity landscape. We then review diversification studies of tropical terrestrial animal and plant clades and discuss three major models of speciation: (i) geographic speciation via vicariance (allopatry); (ii) ecological speciation impacted by climate and geological changes, and (iii) genomic speciation via genome duplication. Geographic speciation has been the most widely documented to date and is a common speciation model across tropical Africa. We conclude with four important challenges faced by tropical African biodiversity research: (i) to increase knowledge by gathering basic and fundamental biodiversity information; (ii) to improve modelling of African geophysical evolution throughout the Cenozoic via better constraints and downscaling approaches; (iii) to increase the precision of phylogenetic reconstruction and molecular dating of tropical African clades by using next generation sequencing approaches together with better fossil calibrations; (iv) finally, as done here, to integrate data better from Earth and life sciences by focusing on the interdisciplinary study of the evolution of tropical African biodiversity in a wider geodiversity context.

Can the genomics of ecological speciation be predicted across the divergence continuum from host races to species? A case study in Rhagoletis.

Studies assessing the predictability of evolution typically focus on short-term adaptation within populations or the repeatability of change among lineages. A missing consideration in speciation research is to determine whether natural selection predictably transforms standing genetic variation within populations into differences between species. Here, we test whether and how host-related selection on diapause timing associates with genome-wide differentiation during ecological speciation by comparing ancestral hawthorn and newly formed apple-infesting host races of Rhagoletis pomonella to their sibling species Rhagoletis mendax that attacks blueberries. The associations of 57 857 single nucleotide polymorphisms in a diapause genome-wide-association study (GWAS) on the hawthorn race strongly predicted the direction and magnitude of genomic divergence among the three fly populations at a field site in Fennville, MI, USA. The apple race and R. mendax show parallel changes in the frequencies of putative inversions on three chromosomes associated with the earlier fruiting times of apples and blueberries compared to hawthorns. A diapause GWAS on R. mendax revealed compensatory changes throughout the genome accounting for the earlier eclosion of blueberry, but not apple flies. Thus, a degree of predictability, although not complete, exists in the genomics of diapause across the ecological speciation continuum in Rhagoletis. The generality of this result is placed in the context of other similar systems. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

The contribution of ancient admixture to reproductive isolation between European sea bass lineages.

Understanding how new species arise through the progressive establishment of reproductive isolation (RI) barriers between diverging populations is a major goal in Evolutionary Biology. An important result of speciation genomics studies is that genomic regions involved in RI frequently harbor anciently diverged haplotypes that predate the reconstructed history of species divergence. The possible origins of these old alleles remain much debated, as they relate to contrasting mechanisms of speciation that are not yet fully understood. In the European sea bass (Dicentrarchus labrax), the genomic regions involved in RI between Atlantic and Mediterranean lineages are enriched for anciently diverged alleles of unknown origin. Here, we used haplotype‐resolved whole‐genome sequences to test whether divergent haplotypes could have originated from a closely related species, the spotted sea bass (Dicentrarchus punctatus). We found that an ancient admixture event between D. labrax and D. punctatus is responsible for the presence of shared derived alleles that segregate at low frequencies in both lineages of D. labrax. An exception to this was found within regions involved in RI between the two D. labrax lineages. In those regions, archaic tracts originating from D. punctatus locally reached high frequencies or even fixation in Atlantic genomes but were almost absent in the Mediterranean. We showed that the ancient admixture event most likely occurred between D. punctatus and the D. labrax Atlantic lineage, while Atlantic and Mediterranean D. labrax lineages were experiencing allopatric isolation. Our results suggest that local adaptive introgression and/or the resolution of genomic conflicts provoked by ancient admixture have probably contributed to the establishment of RI between the two D. labrax lineages.

Contrasting genomic and phenotypic outcomes of hybridization between pairs of mimetic butterfly taxa across a suture zone.

Hybrid zones, whereby divergent lineages come into contact and eventually hybridize, can provide insights on the mechanisms involved in population differentiation and reproductive isolation, and ultimately speciation. Suture zones offer the opportunity to compare these processes across multiple species. In this paper we use reduced-complexity genomic data to compare the genetic and phenotypic structure and hybridization patterns of two mimetic butterfly species, Ithomia salapia and Oleria onega (Nymphalidae: Ithomiini), each consisting of a pair of lineages differentiated for their wing colour pattern and that come into contact in the Andean foothills of Peru. Despite similarities in their life history, we highlight major differences, both at the genomic and phenotypic level, between the two species. These differences include the presence of hybrids, variations in wing phenotype, and genomic patterns of introgression and differentiation. In I.salapia, the two lineages appear to hybridize only rarely, whereas in O.onega the hybrids are not only more common, but also genetically and phenotypically more variable. We also detected loci statistically associated with wing colour pattern variation, but in both species these loci were not over-represented among the candidate barrier loci, suggesting that traits other than wing colour pattern may be important for reproductive isolation. Our results contrast with the genomic patterns observed between hybridizing lineages in the mimetic Heliconius butterflies, and call for a broader investigation into the genomics of speciation in Ithomiini - the largest radiation of mimetic butterflies.

An Improved Genome Assembly for Drosophila navojoa, the Basal Species in the mojavensis Cluster.

Three North American cactophilic Drosophila species, D. mojavensis, D. arizonae, and D. navojoa, are of considerable evolutionary interest owing to the shift from breeding in Opuntia cacti to columnar species. The 3 species form the “mojavensis cluster” of Drosophila. The genome of D. mojavensis was sequenced in 2007 and the genomes of D. navojoa and D. arizonae were sequenced together in 2016 using the same technology (Illumina) and assembly software (AllPaths-LG). Yet, unfortunately, the D. navojoa genome was considerably more fragmented and incomplete than its sister species, rendering it less useful for evolutionary genetic studies. The D. navojoa read dataset does not fully meet the strict insert size required by the assembler used (AllPaths-LG) and this incompatibility might explain its assembly problems. Accordingly, when we re-assembled the genome of D. navojoa with the SPAdes assembler, which does not have the strict AllPaths-LG requirements, we obtained a substantial improvement in all quality indicators such as N50 (from 84 kb to 389 kb) and BUSCO coverage (from 77% to 97%). Here we share a new, improved reference assembly for D. navojoa genome, along with a RNAseq transcriptome. Given the basal relationship of the Opuntia breeding D. navojoa to the columnar breeding D. arizonae and D. mojavensis, the improved assembly and annotation will allow researchers to address a range of questions associated with the genomics of host shifts, chromosomal rearrangements and speciation in this group.

What is Speciation Genomics? The roles of ecology, gene flow, and genomic architecture in the formation of species

What is Speciation Genomics? The roles of ecology, gene flow, and genomic architecture in the formation of species

Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.

Speciation, the evolution of reproductive isolation among populations, is continuous, complex, and involves multiple, interacting barriers. Until it is complete, the effects of this process vary along the genome and can lead to a heterogeneous genomic landscape with peaks and troughs of differentiation and divergence. When gene flow occurs during speciation, barriers restricting gene flow locally in the genome lead to patterns of heterogeneity. However, genomic heterogeneity can also be produced or modified by variation in factors such as background selection and selective sweeps, recombination and mutation rate variation, and heterogeneous gene density. Extracting the effects of gene flow, divergent selection and reproductive isolation from such modifying factors presents a major challenge to speciation genomics. We argue one of the principal aims of the field is to identify the barrier loci involved in limiting gene flow. We first summarize the expected signatures of selection at barrier loci, at the genomic regions linked to them and across the entire genome. We then discuss the modifying factors that complicate the interpretation of the observed genomic landscape. Finally, we end with a road map for future speciation research: a proposal for how to account for these modifying factors and to progress towards understanding the nature of barrier loci. Despite the difficulties of interpreting empirical data, we argue that the availability of promising technical and analytical methods will shed further light on the important roles that gene flow and divergent selection have in shaping the genomic landscape of speciation.