Mutualism with sea anemones triggered the adaptive radiation of clownfishes

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.

Hybridisation and diversification in the adaptive radiation of clownfishes

“…This can originate from the lack of phylogenetic informative sites between closely related species. Previous studies of phylogenetic relationships of the Pomacentridae inferred by mitochondrial or nuclear markers, all support the monophyly of the clownfish as well as the existence of the main clownfish clades [18,[23][24][25]. The topology obtained with the mitochondrial data corresponds to these published phylogenetic trees.…”

“…This behaviour is the key innovation that promoted the adaptive radiation of clownfishes as species segregated among specific combinations of potential host species and habitat, each time matching their phenotype to the environment [18]. While this process of ecological speciation [9] could alone be responsible for the extant diversity of clownfish species, evidence suggests that hybridisation may have occurred during the evolution of the group.…”

Host specialist clownfishes are environmental niche generalists

“…The 28 currently recognized species [16] are obligate mutualists with sea anemones (Anthozoa; Actinaria) and occur throughout the tropical Indian and Pacific Oceans. The ability of clownfishes to be unharmed by the otherwise stinging tentacles of the sea anemone probably triggered the evolutionary radiation of clownfishes [17]. Host specificity varies in clownfishes from interactions with a single host to potentially all the 10 sea anemone species that host clownfishes [16].…”

High Rate of Protein Coding Sequence Evolution and Species Diversification in the Lycaenids

“…They are ubiquitous in nature and often essential for the functioning of ecosystems (Smith and Donoghue, 2008;Yoder et al, 2010). In addition to the ecological benefits of mutualistic interactions for species co-existence and biodiversity (Hoeksema and Kummel, 2003), the apparition of mutualistic interactions has been documented to trigger the diversification of organisms in several clades (Harry et al, 1996;Pellmyr and Krenn, 2002;Litsios et al, 2012). As a consequence, many ecosystems are currently dominated by species involved in one or several mutualistic interactions (Lewinsohn et al, 2006).…”

“…The rate of molecular evolution is also influenced by the generation time of a clade, since the reproduction involves the accumulation of germinal mutations (Gillooly et al, 2005). Classic contrasts in the rate of molecular evolution associated to generation time oppose herbaceous plants to trees (Smith and Donoghue, 2008), small vs. large mammals (Martin and Palumbi, 1993) and birds (Nabholz et al, 2016), or more generally long lived animals contrasted to those with short generation times (Thomas et al, 2010;Litsios et al, 2012). Other life-history traits linked to reproduction such as mating system are associated with the rate of molecular evolution in lineages (Burgarella et al, 2015).…”