Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia)

Abstract

Sexuality and reproductive mode are two fundamental life-history traits that exhibit largely unexplained macroevolutionary patterns among the major groups of multicellular organisms. For example, the cnidarian class Anthozoa (corals and anemones) is mainly comprised of gonochoric (separate sex) brooders or spawners, while one order, Scleractinia (skeleton-forming corals), appears to be mostly hermaphroditic spawners. Here, using the most complete phylogeny of scleractinians, we reconstruct how evolutionary transitions between sexual systems (gonochorism versus hermaphrodism) and reproductive modes (brooding versus spawning) have generated large-scale taxonomic patterns in these characters. Hermaphrodites have independently evolved in three large, distantly related lineages consisting of mostly reef-building species. Reproductive mode in corals has evolved at twice the rate of sexuality, while the evolution of sexuality has been heavily biased: gonochorism is over 100 times more likely to be lost than gained, and can only be acquired by brooders. This circuitous evolutionary pathway accounts for the prevalence of hermaphroditic spawners among reef-forming scleractinians, despite their ancient gonochoric heritage.

Faunal breaks and species composition of Indo-Pacific corals: the role of plate tectonics, environment and habitat distribution

“…Phylogenetic effects, represented by clade nested within suborder, accounted for less than 1 per cent of the variation within the model. However, sexuality, in addition to providing information about colonization potential, is highly conserved within clades [53] and, therefore, may implicitly incorporate a phylogenetic signal. This interpretation is supported by the fact that phylogenetic random effects become more important if sexuality was dropped from the analysis.…”

The reproductive biology of the scleractinian coral Plesiastrea versipora in Sydney Harbour, Australia

“…In contrast to sexuality, the mode of larval development is 4 times more likely to evolve between character states than sexuality (Kerr et al 2011), and therefore, this feature of reproductive biology is less useful as an indicator of evolutionary relationships. Nonetheless, all 3 other species for which the mode of larval development is known in Clade XIV are broadcast spawners (Baird et al 2009b), indicating that spawning is the most likely mode of larval development in Plesiastrea versipora.…”

“…In contrast, colony size was strongly associated with sex, with all colonies greater than 400 cm 2 being male. Sexuality in corals is a highly conserved trait (Harrison 1985, Kerr et al 2011, with very few of the recently defined molecular clades containing species with differing sexuality (Baird et al 2009b, Harrison 2011. This suggests that sexuality is a good character for taxonomic studies.…”

“…Sexuality is also a highly conserved and therefore a good indication of evolutionary relationship (Baird et al 2009b). Similarly, there are only 2 modes of larval development in corals (Kerr et al 2011). Fertilization is either internal with larvae brooded within the polyps, or fertilization is external following the broadcast spawning of gametes (Baird et al 2009b, Harrison 2011.…”

“…Sexual systems in scleractinian corals generally fall into one of 2 categories (Kerr et al 2011). Individual colonies are either hermaphrodites, in which each polyp contains both male and female gametes when mature, or gonochores, in which every polyp in a colony contains either male or female gametes.…”