The genetic mosaic suggests a new role for hitchhiking in ecological speciation

Early in ecological speciation, the genomically localized effects of divergent selection cause heterogeneity among loci in divergence between incipient species. We call this pattern of genomic variability in divergence the 'genetic mosaic of speciation'. Previous studies have used F(ST) outliers as a way to identify divergently selected genomic regions, but the nature of the relationship between outlier loci and quantitative trait loci (QTL) involved in reproductive isolation has not yet been quantified. Here, we show that F(ST) outliers between a pair of incipient species are significantly clustered around QTL for traits that cause ecologically based reproductive isolation. Around these key QTL, extensive 'divergence hitchhiking' occurs because reduced inter-race mating and negative selection decrease the opportunity for recombination between chromosomes bearing different locally adapted QTL alleles. Divergence hitchhiking is likely to greatly increase the opportunity for speciation in populations that are sympatric, regardless of whether initial divergence was sympatric or allopatric. Early in ecological speciation, analyses of population structure, gene flow or phylogeography based on different random or arbitrarily chosen neutral markers should be expected to conflict--only markers in divergently selected genomic regions will reveal the evolutionary history of adaptive divergence and ecologically based reproductive isolation. Species retain mosaic genomes for a very long time, and gene exchange in hybrid zones can vary dramatically among loci. However, in hybridizing species, the genomic regions that affect ecologically based reproductive isolation are difficult to distinguish from regions that have diverged for other reasons.     

Testing the role of climate in speciation: New methods and applications to squamate reptiles (lizards and snakes)

Climate may play important roles in speciation, such as causing the range fragmentation that underlies allopatric speciation (through niche conservatism) or driving divergence of parapatric populations along climatic gradients (through niche divergence). Here, we developed new methods to test the frequency of climate niche conservatism and divergence in speciation, and applied it to species pairs of squamate reptiles (lizards and snakes). We used a large‐scale phylogeny to identify 242 sister species pairs for analysis. From these, we selected all terrestrial allopatric pairs with sufficient occurrence records (n = 49 pairs) and inferred whether each originated via climatic niche conservatism or climatic niche divergence. Among the 242 pairs, allopatric pairs were most common (41.3%), rather than parapatric (19.4%), partially sympatric (17.7%), or fully sympatric species pairs (21.5%). Among the 49 selected allopatric pairs, most appeared to have originated via climatic niche divergence (61–76%, depending on the details of the methods). Surprisingly, we found greater climatic niche divergence between allopatric sister species than between parapatric pairs, even after correcting for geographic distance. We also found that niche divergence did not increase with time, further implicating niche divergence in driving lineage splitting. Overall, our results suggest that climatic niche divergence may often play an important role in allopatric speciation, and the methodology developed here can be used to address the generality of these findings in other organisms.     

Combining Biogeographic and Phylogenetic Data to Examine Primate Speciation: An Example Using Cercopithecin Monkeys

We combined phylogenetic and biogeographic data to examine the mode of speciation in a group of African monkeys, the Cercopithecini. If allopatric speciation is the major force producing species, then there should be a positive relationship between the relative divergence time of taxa and their degree of geographic range overlap. Alternatively, an opposite relationship between divergence time and geographic range overlap is consistent with sympatric speciation as the main mechanism underlying the cercopithecin radiation. We collected biogeographic and phylogenetic data for 19 guenon species from the literature. We digitized geographic range maps and utilized three different phylogenetic hypotheses based on Y chromosome, X chromosome, and mitochondrial (mtDNA) data. We used regressions with Monte Carlo simulation to examine the relationship between the relative time since divergence of taxa and their degree of geographic range overlap. We found that there was a positive relationship between relative divergence time and the proportion of geographic range overlap between taxa using all three molecular data sets. Our findings provide evidence for allopatric speciation being the common mode of diversification in the cercopithecin clade. Because most of these primates are forest adapted mammals, the cyclical contraction and expansion of African forests from the late Miocene to the present has likely been an important factor driving allopatric speciation. In addition, geographic barriers such as the Congo and Sanaga rivers have probably played a complementary role in producing new species within the clade.     

Genomic signatures of divergent selection and speciation patterns in a ‘natural experiment’, the young parallel radiations of Nicaraguan crater lake cichlid fishes

Divergent selection is the main driving force in sympatric ecological speciation and may also play a strong role in divergence between allopatric populations. Characterizing the genome‐wide impact of divergent selection often constitutes a first step in unravelling the genetic bases underlying adaptation and ecological speciation. The Midas cichlid fish (Amphilophus citrinellus) species complex in Nicaragua is a powerful system for studying evolutionary processes. Independent colonizations of isolated young crater lakes by Midas cichlid populations from the older and great lakes of Nicaragua resulted in the repeated evolution of adaptive radiations by intralacustrine sympatric speciation. In this study we performed genome scans on two repeated radiations of crater lake species and their great lake source populations (1030 polymorphic AFLPs, n ～ 30 individuals per species). We detected regions under divergent selection (0.3% in the crater lake Xiloá flock and 1.7% in the older crater lake Apoyo radiation) that might be responsible for the sympatric diversifications. We find no evidence that the same genomic regions have been involved in the repeated evolution of parallel adaptations across crater lake flocks. However, there is some genetic parallelism apparent (seven out of 51 crater lake to great lake outlier loci are shared; 13.7%) that is associated with the allopatric divergence of both crater lake flocks. Interestingly, our results suggest that the number of outlier loci involved in sympatric and allopatric divergence increases over time. A phylogeny based on the AFLP data clearly supports the monophyly of both crater lake species flocks and indicates a parallel branching order with a primary split along the limnetic‐benthic axis in both radiations.     

Genomic signatures of rapid adaptive divergence in a tropical montane species

Mountain regions contain extraordinary biodiversity. The environmental heterogeneity and glacial cycles often accelerate speciation and adaptation of montane species, but how these processes influence the genomic differentiation of these species is largely unknown. Using a novel chromosome-level genome and population genomic comparisons, we study allopatric divergence and selection in an iconic bird living in a tropical mountain region in New Guinea, Archbold''s bowerbird (Amblyornis papuensis). Our results show that the two populations inhabiting the eastern and western Central Range became isolated ca 11 800 years ago, probably because the suitable habitats for this cold-tolerating bird decreased when the climate got warmer. Our genomic scans detect that genes in highly divergent genomic regions are over-represented in developmental processes, which is probably associated with the observed differences in body size between the populations. Overall, our results suggest that environmental differences between the eastern and western Central Range probably drive adaptive divergence between them.     

Molecular correlates of reproductive isolation

Evolution of reproductive isolation as a byproduct of genetic divergence in isolated populations is the dominant (albeit not exclusive) mode of speciation in sexual animals. But little is known about the factors linking speciation to general divergence. Several authors have argued that allopatric speciation should proceed more rapidly if isolated populations also experience divergent selection. Reproductive isolation between allopatric populations is not subject to direct selection; it can accumulate only by random drift or as a fortuitous byproduct of selection on other traits. Here I present a novel analysis of published data, demonstrating that pre- and postmating isolation of Drosophila species are more tightly correlated with allozyme divergence than with silent DNA divergence. Inasmuch as proteins are more subject to the action of natural selection than are silent DNA polymorphisms, this result provides broad support for a model of selection-mediated allopatric speciation.     

LATITUDINAL VARIATION IN SPECIATION MECHANISMS IN FROGS

Speciation often has a strong geographical and environmental component, but the ecological factors that potentially underlie allopatric and parapatric speciation remain understudied. Two ecological mechanisms by which speciation may occur on geographic scales are allopatric speciation through niche conservatism and parapatric or allopatric speciation through niche divergence. A previous study on salamanders found a strong latitudinal pattern in the prevalence of these mechanisms, with niche conservatism dominating in temperate regions and niche divergence dominating in the tropics, and related this pattern to Janzen's hypothesis of greater climatic zonation between different elevations in the tropics. Here, we test for latitudinal patterns in speciation in a related but more diverse group of amphibians, the anurans. Using data from up to 79 sister-species pairs, we test for latitudinal variation in elevational and climatic overlap between sister species, and evaluate the frequency of speciation via niche conservatism versus niche divergence in relation to latitude. In contrast to salamanders, we find no tendency for greater niche divergence in the tropics or for greater niche conservatism in temperate regions. Although our results support the idea of greater climatic zonation in tropical regions, they show that this climatic pattern does not lead to straightforward relationships between speciation, latitude, and niche evolution.     

Evolution of noncoding and silent coding sites in the Plasmodium falciparum and Plasmodium reichenowi genomes

We compared levels of sequence divergence between fourfold synonymous coding sites and noncoding sites from the intergenic and intronic regions of the Plasmodium falciparum and Plasmodium reichenowi genomes. We observed significant differences in the level of divergence between these classes of silent sites. Fourfold synonymous coding sites exhibited the highest level of sequence divergence, followed by introns, and then intergenic sequences. This pattern of relative divergence rates has been observed in primate genomes but was unexpected in Plasmodium due to a paucity of variation at silent sites in P. falciparum and the corollary hypothesis that silent sites in this genome may be subject to atypical selective constraints. Exclusion of hypermutable CpG dinucleotides reduces the divergence level of synonymous coding sites to that of intergenic sites but does not diminish the significantly higher divergence level of introns relative to intergenic sites. A greater than expected incidence of CpG dinucleotides in intergenic regions less than 500 bp from genes may indicate selective maintenance of regulatory motifs containing CpGs. Divergence rates of different classes of silent sites in these Plasmodium genomes are determined by a combination of mutational and selective pressures.     

Tracking the progression of speciation: variable patterns of introgression across the genome provide insights on the species delimitation between progenitor–derivative spruces (Picea mariana × P. rubens)

The genic species concept implies that while most of the genome can be exchanged somewhat freely between species through introgression, some genomic regions remain impermeable to interspecific gene flow. Hence, interspecific differences can be maintained despite ongoing gene exchange within contact zones. This study assessed the heterogeneous patterns of introgression at gene loci across the hybrid zone of an incipient progenitor–derivative species pair, Picea mariana (black spruce) and Picea rubens (red spruce). The spruce taxa likely diverged in geographic isolation during the Pleistocene and came into secondary contact during late Holocene. A total of 300 SNPs distributed across the 12 linkage groups (LG) of black spruce were genotyped for 385 individual trees from 33 populations distributed across the allopatric zone of each species and within the zone of sympatry. An integrative framework combining three population genomic approaches was used to scan the genomes, revealing heterogeneous patterns of introgression. A total of 23 SNPs scattered over 10 LG were considered impermeable to introgression and putatively under diverging selection. These loci revealed the existence of impermeable genomic regions forming the species boundary and are thus indicative of ongoing speciation between these two genetic lineages. Another 238 SNPs reflected selectively neutral diffusion across the porous species barrier. Finally, 39 highly permeable SNPs suggested ancestral polymorphism along with balancing selection. The heterogeneous patterns of introgression across the genome indicated that the speciation process between black spruce and red spruce is young and incomplete, albeit some interspecific differences are maintained, allowing ongoing species divergence even in sympatry. The approach developed in this study can be used to track the progression of ongoing speciation processes.     

Genetic divergence within the monotypic tree genus <Emphasis Type="Italic">Platycarya</Emphasis> (Juglandaceae) and its implications for species’ past dynamics in subtropical China

Subtropical East Asia harbours a large plant diversity that is often attributed to allopatric speciation in this topographically complex region characterized by a relative climate stability. Here, we use observations of Platycarya, a widespread subtropical Asian tree genus, to explore the consequences of past climate stability on species’ evolutionary history in subtropical China. This genus has a controversial taxonomy: while it is now prevailingly treated as monotypic, two species have been originally described, Platycarya strobilacea and P. longipes. Previous information from species distribution models, fossil pollen data and genetic data based on chloroplast DNA (cpDNA) were integrated with newly obtained genetic data from the two putative species. We used both cpDNA (psbA-trnH and trnL-F intergenic spacers, including a partial trnL gene sequence) and nuclear markers. The latter included sequences of the internal transcribed spacer region (ITS1–5.8S–ITS2) of the nuclear ribosomal DNA and random genomic single nucleotide polymorphisms. Using these nuclear genetic markers, we found interspecific genetic divergence fitting with the ‘two species’ scenario and geographically structured intraspecific variation. Using cpDNA markers, we also found geographically structured intraspecific variation. Despite deep inter- and intraspecific genetic divergence, we detected genetic admixture in southwest China. Overall, our findings of genetic divergence within Platycarya support the hypothesis of allopatric speciation. However, episodes of population interconnection were identified, at least in southwest China, suggesting that the genus has had a dynamic population history.     

Inter‐specific gene flow dynamics during the Pleistocene‐dated speciation of forest‐dependent mosquitoes in Southeast Asia

Tropical forests have undergone repeated fragmentation and expansion during Pleistocene glacial and interglacial periods, respectively. The effects of this repeated forest fragmentation in driving vicariance in tropical taxa have been well studied. However, relatively little is known about how often this process results in allopatric speciation, since it may be inhibited by recurrent gene flow during repeated secondary contact, or to what extent Pleistocene‐dated speciation results from ecological specialization in the face of gene flow. Here, divergence times and gene flow between three closely‐related mosquito species of the Anopheles dirus species complex endemic to the forests of Southeast Asia, are inferred using coalescent based Bayesian analysis. An Isolation with Migration model is applied to sequences of two mitochondrial and three nuclear genes, and 11 microsatellites. The divergence of An. scanloni has occurred despite unidirectional nuclear gene flow from this species into An. dirus. The inferred asymmetric gene flow may result from the unique evolutionary adaptation of An. scanloni to limestone karst habitat, and therefore the fitness advantage of this species over An. dirus in regions of sympatry. Mitochondrial introgression has led to the complete replacement of An. dirus haplotypes with those of An. baimaii through a recent (～62 kya) selective sweep. Speciation of An. baimaii and An. dirus is inferred to have involved allopatric divergence throughout much of the Pleistocene. Secondary contact and bidirectional gene flow has occurred only within the last 100 000 years, by which time the process of allopatric speciation seems to have been largely completed.     

The geographical pattern of speciation and floral diversification in the neotropics: the tribe sinningieae (gesneriaceae) as a case study

The geographical pattern of speciation and the relationship between floral variation and species ranges were investigated in the tribe Sinningieae (Gesneriaceae), which is found mainly in the Atlantic forests of Brazil. Geographical distribution data recorded on a grid system of 0.5 x 0.5 degree intervals and a near-complete species-level phylogenetic tree of Sinningieae inferred from a simultaneous analysis of seven DNA regions were used to address the role of geographical isolation in speciation. Geographical range overlaps between sister lineages were measured across all nodes in the phylogenetic tree and analyzed in relation to relative ages estimated from branch lengths. Although there are several cases of species sympatry in Sinningieae, patterns of sympatry between sister taxa support the predominance of allopatric speciation. The pattern of sympatry between sister taxa is consistent with range shifts following allopatric speciation, except in one clade, in which the overlapping distribution of recent sister species indicates speciation within a restricted geographical area and involving changes in pollinators and habitats. The relationship between floral divergence and regional sympatry was also examined by analyzing floral contrasts, phenological overlap, and the degree of sympatry between sister clades. Morphological contrast between flowers is not increased in sympatry and phenological divergence is more apparent between allopatric clades than between sympatric clades. Therefore, our results failed to indicate a tendency for sympatric taxa to minimize morphological and phenological overlap (geographic exclusion and/or character displacement hypotheses). Instead, they point toward adaptation in phenology to local conditions and buildup of sympatries at random with respect to flower morphology. Additional studies at a lower geographical scale are needed to identify truely coexisting species and the components of their reproductive isolation.     

Genome-wide patterns of divergence during speciation: the lake whitefish case study

The nature, size and distribution of the genomic regions underlying divergence and promoting reproductive isolation remain largely unknown. Here, we summarize ongoing efforts using young (12 000 yr BP) species pairs of lake whitefish (Coregonus clupeaformis) to expand our understanding of the initial genomic patterns of divergence observed during speciation. Our results confirmed the predictions that: (i) on average, phenotypic quantitative trait loci (pQTL) show higher F(ST) values and are more likely to be outliers (and therefore candidates for being targets of divergent selection) than non-pQTL markers; (ii) large islands of divergence rather than small independent regions under selection characterize the early stages of adaptive divergence of lake whitefish; and (iii) there is a general trend towards an increase in terms of numbers and size of genomic regions of divergence from the least (East L.) to the most differentiated species pair (Cliff L.). This is consistent with previous estimates of reproductive isolation between these species pairs being driven by the same selective forces responsible for environment specialization. Altogether, dwarf and normal whitefish species pairs represent a continuum of both morphological and genomic differentiation contributing to ecological speciation. Admittedly, much progress is still required to more finely map and circumscribe genomic islands of speciation. This will be achieved through the use of next generation sequencing data but also through a better quantification of phenotypic traits moulded by selection as organisms adapt to new environmental conditions.     

Gene duplication and mobile genetic elements in the morning glories

We review gene duplication and subsequent structural and functional divergence in the anthocyanin biosynthesis genes in the Japanese and common morning glories and discuss their evolutionary implications. These plants appear to contain at least six copies of the CHS gene and three tandem copies of the DFR gene. Of these, the CHS-D and DFR-B genes are mainly responsible for flower pigmentation and mutations in these genes confer white flowers. We compared the genomic sequences of these duplicated genes between the two morning glories and found small mobile element-like sequences (MELSs) and direct repeats (DRs) in introns and intergenic regions. The results indicate that the MELS elements and DRs play significant roles in divergence after gene duplication. We also discuss DNA rearrangements occurring before and after speciation of these morning glories. DNA transposable elements belonging to the Ac/Ds or En/Spm families have acted as major spontaneous mutagens in these morning glories. We also describe the structural features of the first Mu-related element found in the morning glories and polymorphisms found in the same species.     

Consequences of divergence and introgression for speciation in Andean cloud forest birds

Divergence with gene flow is well documented and reveals the influence of ecological adaptation on speciation. Yet, it remains intuitive that gene exchange inhibits speciation in many scenarios, particularly among ecologically similar populations. The influence of gene flow on the divergence of populations facing similar selection pressures has received less empirical attention than scenarios where differentiation is coupled with local environmental adaptation. I used a paired study design to test the influence of genomic divergence and introgression on plumage differentiation between ecologically similar allopatric replacements of Andean cloud forest birds. Through analyses of short‐read genome‐wide sequences from over 160 individuals in 16 codistributed lineages, I found that plumage divergence is associated with deep genetic divergence, implicating a prominent role of geographic isolation in speciation. By contrast, lineages that lack plumage divergence across the same geographic barrier are more recently isolated or exhibit a signature of secondary genetic introgression, indicating a negative relationship between gene flow and divergence in phenotypic traits important to speciation. My results suggest that the evolutionary outcomes of cycles of isolation and divergence in this important theatre of biotic diversification are sensitive to time spent in the absence of gene flow.     

Divergence between the Drosophila pseudoobscura and D. persimilis genome sequences in relation to chromosomal inversions

As whole-genome sequence assemblies accumulate, a challenge is to determine how these can be used to address fundamental evolutionary questions, such as inferring the process of speciation. Here, we use the sequence assemblies of Drosophila pseudoobscura and D. persimilis to test hypotheses regarding divergence with gene flow. We observe low differentiation between the two genome sequences in pericentromeric and peritelomeric regions. We interpret this result as primarily a remnant of the correlation between levels of variation and local recombination rate observed within populations. However, we also observe lower differentiation far from the fixed chromosomal inversions distinguishing these species and greater differentiation within and near these inversions. This finding is consistent with models suggesting that chromosomal inversions facilitate species divergence despite interspecies gene flow. We also document heterogeneity among the inverted regions in their degree of differentiation, suggesting temporal differences in the origin of each inverted region consistent with the inversions arising during a process of divergence with gene flow. While this study provides insights into the speciation process using two single-genome sequences, it was informed by lower throughput but more rigorous examinations of polymorphism and divergence. This reliance highlights the need for complementary genomic and population genetic approaches for tackling fundamental evolutionary questions such as speciation.     

Evolution of three Pyrenophora cereal pathogens: Recent divergence, speciation and evolution of non-coding DNA

Three of the most important fungal pathogens of cereals are Pyrenophora tritici-repentis, the cause of tan spot on wheat, and Pyrenophora teres f. teres and Pyrenophora teres f. maculata, the cause of spot form and net form of net blotch on barley, respectively. Orthologous intergenic regions were used to examine the genetic relationships and divergence times between these pathogens. Mean divergence times were calculated at 519kya (±30) between P. teresf. teres and P. teresf. maculata, while P. tritici-repentis diverged from both Pyrenophora teresforms 8.04Mya (±138ky). Individual intergenic regions showed a consistent pattern of co-divergence of the P. teresforms from P. tritici-repentis, with the pattern supported by phylogenetic analysis of conserved genes. Differences in calculated divergence times between individual intergenic regions suggested that they are not entirely under neutral selection, a phenomenon shared with higher Eukaryotes. P. tritici-repentis regions varied in divergence time approximately 5-12Mya from the P. teres lineage, compared to the separation of wheat and barley some 12Mya, while the P. teresf. teres and P. teresf. maculata intergenic region divergences correspond to the middle Pleistocene. The data suggest there is no correlation between the divergence of these pathogens the domestication of wheat and barley, and show P. teresf. teres and P. teresf. maculata are closely related but autonomous. The results are discussed in the context of speciation and the evolution of intergenic regions.     

Microgeographic evolution of snail shell shape and predator behavior

Genetic divergence in geographically isolated populations is a prerequisite for allopatric speciation, one of the most common modes of speciation. In ecologically equivalent populations existing within a small, environmentally homogeneous area, an important role for environmentally neutral divergence is often found or inferred. We studied a species complex of conspicuously shaped Opisthostoma land snails on scattered limestone outcrops within a small area of lowland rainforest in Borneo. We used shell morphometrics, mitochondrial and nuclear DNA sequences, and marks of predation to study the factors involved in allopatric divergence. We found that a striking geographic divergence exists in shell morphology, which is partly associated with neutral genetic divergence. We also found geographic differentiation in the behavior of the snails' invertebrate predator and evidence of an evolutionary interaction between aspects of shell shape and predator behavior. Our study shows that adaptation to biotic aspects of the environment may play a more important role in allopatric speciation than previously suspected, even on a geographically very small scale.