Live fast, diversify non-adaptively: evolutionary diversification of exceptionally short-lived annual killifishes

Abstract

BackgroundAdaptive 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.ResultsNothobranchius 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.ConclusionsNothobranchius 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.Electronic supplementary materialThe online version of this article (10.1186/s12862-019-1344-0) contains supplementary material, which is available to authorized users.

Genetic diversity of a widespread annual killifish from coastal Tanzania

“…The region experiences much longer duration of the wet phase, with two rainy seasons each year and a longer duration of habitat inundation compared to a single rainy season in subtropical Mozambique [41] with very brief periods of inundation [42,43]. It demonstrates that Nothobranchius fishes experience variable climatic and ecological challenges that may affect their dispersal, diversification and coexistence in local killifish assemblages [44].…”

“…Nothobranchius populations are finely structured in small, short-existing pools in dry inland region of southern Mozambique [14,42] where main river channels form significant barriers to dispersal and lead to allopatric species and strong intra-specific diversification [15]. In contrast, humid equatorial region appears to enable greater dispersal across river channels and between river basins ( [5,10,44], present study), with Nothobranchius fishes occurring in extensive marshes and semipermanent streams [5,16,57]. Nothobranchius fishes are also present in the elevated part of equatorial East Africa (> 800 masl) and it remains to be tested how local populations are structured there.…”

Accelerated Brain Shape Evolution Is Associated with Rapid Diversification in an Avian Radiation

“…This could promote diversification if niche divergence results in reproductive isolation among populations (Nosil 2012). Alternatively, brain morphologies in kingfishers, if linked to frequent behavioral innovations (Sol et al 2005a) or patterns that govern dispersal (Sol et al 2010), could drive rapid speciation on islands (Andersen et al 2018) through enabling clades to take advantage of ecological or "spatial" opportunity (sensu Lambert et al 2019) available in island archipelagos that causes genetic divergence between populations (Price 2008). Indeed, the two kingfisher subclades with the fastest diversification rates, Todiramphus and Ceyx (Andersen et al 2018), also have the highest rates of brain shape evolution (fig.…”

Trait evolution and historical biogeography shape assemblages of annual killifish

“…A study of 48 species in the comparable African annual killifish genus Nothobranchius showed that most assemblages showed little variation in body size and only a single group of coexisting species exhibited size differences that may have been the result of ecological character displacement (Lambert, Reichard, & Pincheira-Donoso, 2019). In the La Plata and Patos Lagoon areas small, similar-sized Austrolebias species co-occur ( Figure 1), along with the larger species.…”