Mutualism with sea anemones triggered the adaptive radiation of clownfishes

Abstract

Background: Adaptive 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.

Results: We 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.

Conclusions: The 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.

Figure 1

Clownfishes and sea anemones mutualism, and geographic distribution. Illustration of the mutualistic relationship between Amphiprion chrysopterus and Heteractis crispa(A). The distribution of the damselfishes in blue and of the clownfishes in orange is shown in panel B. As for every clownfish species, the female Amphiprion percula (on top of the picture of panel C, here with Stichodactyla gigantea) is bigger than the male beneath.

Figure 2

Pomacentridae maximum credibility chronogram. Outgroup taxa are shown in black, damselfishes in blue and clownfishes in orange. Error bars on node show the dating confidence intervals, scale is in MY. Numbers above nodes indicate Bayesian posterior probabilities.

Figure 3

Diversification analysis. Rates of speciation, extinction and diversification measured on the sample of 100 chronograms. Rates of damselfishes (mean diversification rate = 0.09) are shown in blue and clownfishes (mean diversification rate = 0.14) in orange.

Figure 4

MCA of mutualistic interactions (axes 1 and 2). Each pie represent a clownfish species and the filling colours correspond to the interacting sea anemone species (see legend in figure). Abbreviations: Amphiprion: A, Premnas: P, Stichodactyla: S, Entacmaea: E, Macrodactyla: M, Heteractis: H, Cryptodendrum: C.

Figure 5

MCA of mutualistic interactions (axes 3 and 4). Legend as in Figure  4.

Figure 6

Rate of morphological evolution. Evolution of the morphological traits measured on the sample of 100 phylograms (A) and chronograms (B). Rates of clownfishes are in orange, damselfishes in blue and the one-rate model is shown in white. The P-values of model comparison by likelihood ratio test is signified by asterisk (* = P-values <0.05, ** = P-values <0.01). The schematic position of each morphological trait is shown on the clownfish drawing.

Figure 7

Chronogram of the clownfishes radiation. Branch lengths are given in MY. The interacting sea anemone species are shown for each clownfish species. Sea anemone names abbreviations as in Figure  5.