speciation continuum
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Even though speciation involving multiple interacting partners, such as plants and their pollinators, has attracted much research, most studies focus on isolated phases of the process. This currently precludes an integrated understanding of the mechanisms leading to cospeciation. Here, we examine population genetic structure across six species-pairs of figs and their pollinating wasps along an elevational gradient in New Guinea. Specifically, we test three hypotheses on the genetic structure within the examined species-pairs and find that the hypothesized genetic structures represent different phases of a single continuum, from incipient cospeciation to the full formation of new species. Our results also illuminate the mechanisms governing cospeciation, namely that fig wasps tend to accumulate population genetic differences faster than their figs, which initially decouples the speciation dynamics between the two interacting partners and breaks down their one-to-one matching. This intermediate phase is followed by genetic divergence of both partners, which may eventually restore the one-to-one matching among the fully formed species. Together, these findings integrate current knowledge on the mechanisms operating during different phases of the cospeciation process. They also reveal that the increasingly reported breakdowns in one-to-one matching may be an inherent part of the cospeciation process. Mechanistic understanding of this process is needed to explain how the extraordinary diversity of species, especially in the tropics, has emerged. Knowing which breakdowns in species interactions are a natural phase of cospeciation and which may endanger further generation of diversity seems critical in a constantly changing world.
Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d(xy) and relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.
- MeSH
- druhová specificita MeSH
- genom MeSH
- genomika MeSH
- genotypizační techniky MeSH
- jednonukleotidový polymorfismus MeSH
- Passeriformes klasifikace genetika MeSH
- populační genetika MeSH
- rekombinace genetická * MeSH
- reprodukční izolace MeSH
- sekvenční analýza DNA MeSH
- selekce (genetika) * MeSH
- tok genů MeSH
- vznik druhů (genetika) * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: Adaptive radiations are triggered by ecological opportunity - the access to novel niche domains with abundant available resources that facilitate the formation of new ecologically divergent species. Therefore, as new species saturate niche space, clades experience a diversity-dependent slowdown of diversification over time. At the other extreme of the radiation continuum, non-adaptively radiating lineages undergo diversification with minimal niche differentiation when 'spatial opportunity' (i.e. areas with suitable 'ancestral' ecological conditions) is available. Traditionally, most research has focused on adaptive radiations, while empirical studies on non-adaptive radiations remain lagging behind. A prolific clade of African fish with extremely short lifespan (Nothobranchius killifish), show the key evolutionary features of a candidate non-adaptive radiation - primarily allopatric species with minimal niche and phenotypic divergence. Here, we test the hypothesis that Nothobranchius killifish have non-adaptively diversified. We employ phylogenetic modelling to investigate the tempo and mode of macroevolutionary diversification of these organisms. RESULTS: Nothobranchius diversification has proceeded with minor niche differentiation and minimal morphological disparity among allopatric species. Additionally, we failed to identify evidence for a role of body size or biogeography in influencing diversification rates. Diversification has been homogeneous within this genus, with the only hotspot of species-richness not resulting from rapid diversification. However, species in sympatry show higher disparity, which may have been caused by character displacement among coexisting species. CONCLUSIONS: Nothobranchius killifish have proliferated following the tempo and mode of a non-adaptive radiation. Our study confirms that this exceptionally short-lived group have diversified with minimal divergent niche adaptation, while one group of coexisting species seems to have facilitated spatial overlap among these taxa via the evolution of ecological character displacement.
- MeSH
- biodiverzita * MeSH
- biologická evoluce * MeSH
- druhová specificita MeSH
- Fundulidae fyziologie MeSH
- fylogeneze MeSH
- fylogeografie MeSH
- fyziologická adaptace * MeSH
- pravděpodobnostní funkce MeSH
- velikost těla MeSH
- vznik druhů (genetika) MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
