Gaboriau, T. N. | Search bioRxiv

bioRxiv2024

Host-use Drives Convergent Evolution in Clownfish and Disentangles the Mystery of an Iconic Adaptive Radiation

Clownfishes (Amphiprioninae) are a fascinating example of marine radiation. From a central Pacific ancestor, they quickly colonized the coral reefs of the Indo-Pacific and diversified independently on each side of the Indo-Australian Archipelago. Their association with venomous sea anemones is often thought to be the key innovation that enabled the clownfish radiation. However, this intuition has little empirical or theoretical support given our current knowledge of the clade. To date, no ecological variable has been identified that can explain clownfish niche partitioning, phenotypic evolution, species co-occurrence, and thus, the adaptive radiation of the group. Our synthetic work solves this long-standing mystery by testing the influence of sea anemone host use on phenotypic divergence. We provide the first major revision to the known clownfish-sea anemone host associations in over 30 years, accounting for host associations in a biologically relevant way. We gathered whole-genome data for all 28 clownfish species and reconstructed a fully supported species tree for the Amphiprioninae. Integrating this new data into comparative phylogenomic approaches, we demonstrate for the first time, that the host sea anemones are the drivers of convergent evolution in clownfish color pattern and morphology. During the adaptive radiation of this group, clownfishes in different regions that associate with the same hosts have evolved the same phenotypes. Comparative genomics also reveals several genes under convergent positive selection linked to host specialisation events. Our results identify the sea anemone host as the key ecological variable that disentangles the entire adaptive radiation. As one of the most recognizable animals on the planet and an emerging model organism in the biological sciences, our findings bear on the interpretation of dozens of prior studies on clownfishes and will radically reshape research agendas for these iconic organisms.

evolutionary biology↗

bioRxiv2023

Exploring the Macroevolutionary Signature of Asymmetric Inheritance at Speciation

AO_SCPLOWBSTRACTC_SCPLOWPopular comparative phylogenetic models such as Brownian Motion, Ornstein-Ulhenbeck, and their extensions, assume that, at speciation, a trait value is inherited identically by the two descendant species. This assumption contrasts with models of speciation at the micro-evolutionary scale where phenotypic distributions of the descendants are sub-samples of the ancestral distribution. Various described mechanisms of speciation can lead to a displacement of the ancestral phenotypic mean among descendants and an asymmetric inheritance of the ancestral phenotypic variance. In contrast, even macro-evolutionary models that account for intraspecific variance assume symmetrically conserved inheritance of the ancestral phenotypic distribution at speciation. Here we develop an Asymmetric Brownian Motion model (ABM) that relaxes the hypothesis of symmetric and conserved inheritance of the ancestral distribution at the time of speciation. The ABM jointly models the evolution of both intra- and inter-specific phenotypic variation. It also allows the mode of phenotypic inheritance at speciation to be inferred, ranging from a symmetric and conserved inheritance, where descendants inherit the ancestral distribution, to an asymmetric and displaced inheritance, where descendants inherit divergent phenotypic means and variances. To demonstrate this model, we analyze the evolution of beak morphology in Darwin finches, finding evidence of character displacement at speciation. The ABM model helps to bridge micro- and macro-evolutionary models of trait evolution by providing a more robust framework for testing the effects of ecological speciation, character displacement, and niche partitioning on trait evolution at the macro-evolutionary scale.

evolutionary biology↗