Mutualism with sea anemones triggered the adaptive radiation of clownfishes

Glenn Litsios,Peter B Pearman,Niklaus E Zimmermann,Rafael O Wüest,Nicolas Salamin,Carrie A Sims

doi:10.1186/1471-2148-12-212

Abstract

BackgroundAdaptive radiation is the process by which a single ancestral species diversifies into many descendants adapted to exploit a wide range of habitats. The appearance of ecological opportunities, or the colonisation or adaptation to novel ecological resources, has been documented to promote adaptive radiation in many classic examples. Mutualistic interactions allow species to access resources untapped by competitors, but evidence shows that the effect of mutualism on species diversification can greatly vary among mutualistic systems. Here, we test whether the development of obligate mutualism with sea anemones allowed the clownfishes to radiate adaptively across the Indian and western Pacific oceans reef habitats.ResultsWe show that clownfishes morphological characters are linked with ecological niches associated with the sea anemones. This pattern is consistent with the ecological speciation hypothesis. Furthermore, the clownfishes show an increase in the rate of species diversification as well as rate of morphological evolution compared to their closest relatives without anemone mutualistic associations.ConclusionsThe effect of mutualism on species diversification has only been studied in a limited number of groups. We present a case of adaptive radiation where mutualistic interaction is the likely key innovation, providing new insights into the mechanisms involved in the buildup of biodiversity. Due to a lack of barriers to dispersal, ecological speciation is rare in marine environments. Particular life-history characteristics of clownfishes likely reinforced reproductive isolation between populations, allowing rapid species diversification.

Highlights

Adaptive radiation is the process by which a single ancestral species diversifies into many descendants adapted to exploit a wide range of habitats
We inferred a root age of ~19 million years (MY) for the clownfish clade and found the crown Amphiprion group, which holds most of the clownfishes species (25 out of 30 species), to have an age of ~7 MY (Figure 2).We did not include in this divergence time analysis the closure of the Isthmus of Panama
We found that clownfishes exhibit patterns that are likely diagnostic of an ecological adaptive radiation via ecological speciation [4]

Summary

Introduction

Adaptive radiation is the process by which a single ancestral species diversifies into many descendants adapted to exploit a wide range of habitats. Mutualistic interactions allow species to access resources untapped by competitors, but evidence shows that the effect of mutualism on species diversification can greatly vary among mutualistic systems. The appearance of a trait allowing new interactions with the environment, or key innovation, can create an opportunity for species radiation [9]. While a plethora of case studies showing adaptive radiation driven by ecological opportunity offered by one of the aforementioned possibilities exist [9], examples involving mutualism are scarce (but see [12]). Since hosts shifts have allowed ecological speciation in a wide range of organisms, including coraldwelling fish [13,14], there is a possibility for ecological speciation to occur in mutualistic systems. The topic is still debated and in need of further case studies

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