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

Joshua W Lambert,Daniel Pincheira-Donoso,Martin Reichard

doi:10.1186/s12862-019-1344-0

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.

Highlights

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
These data were obtained from extensive field records collected over the course of 10 years by one of us (MR, [45]), as well as from coordinates recorded by overlapping the maps published by Wildekamp [46] with a Phylogenetic tree Macroevolutionary phylogenetic analyses of diversification were performed on a time-calibrated molecular phylogenetic tree that includes 49 of the 71 documented Nothobranchius species from Dorn et al [37] (Additional file 5; [39])
The Monte Carlo Constant Rate (MCCR) analysis found a critical value to reject a pure-birth model of − 2.298, the γ statistic is highly non-significant (p = 0.731, 95% CI one-tailed test), rejecting an early- or late-burst of diversification

Summary

Introduction

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. Evolutionary radiations are not exclusively adaptive [13], and can take place when species diversify with retention of the ancestral niche [14] During this process of non-adaptive radiation [15], episodes of speciation are not the result of divergent natural selection and newly emerging species remain ecologically and phenotypically similar [16]. Lambert et al BMC Evolutionary Biology (2019) 19:10 in contrast to adaptive radiations, diversification via non-adaptive radiation is more likely to take place when newly emerging species radiate across geographically non-overlapping areas (allopatry), which can accommodate species with fundamentally similar niche demands [15, 17, 18] The availability of such areas equipped with suitable ‘ancestral’ ecological conditions is what we refer to as ‘spatial opportunity’. Depending on the availability of vacant ancestral niches, non-adaptive radiations may diversify under a range of radiation trajectories

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Results

Conclusion