Viviparity stimulates diversification in an order of fish

Abstract

Species richness is distributed unevenly across the tree of life and this may be influenced by the evolution of novel phenotypes that promote diversification. Viviparity has originated ∼150 times in vertebrates and is considered to be an adaptation to highly variable environments. Likewise, possessing an annual life cycle is common in plants and insects, where it enables the colonization of seasonal environments, but rare in vertebrates. The extent to which these reproductive life-history traits have enhanced diversification and their relative importance in the process remains unknown. We show that convergent evolution of viviparity causes bursts of diversification in fish. We built a phylogenetic tree for Cyprinodontiformes, an order in which both annualism and viviparity have arisen, and reveal that while both traits have evolved multiple times, only viviparity played a major role in shaping the patterns of diversity. These results demonstrate that changes in reproductive life-history strategy can stimulate diversification.

Figure 1. Phylogenetic tree of Cyprinodontiformes.

A Bayesian maximum clade credibility tree is shown with ancestral reconstructed states of viviparity and annualism. Pie charts in each node represent MuSSE reconstructed ancestral states (NAO, non-annual oviparous). Branches on which BAMM indicated large support for rate changes (Bayes factor >20) are highlighted in colour. Stars denote the node from which clade diversification rates over time were calculated (shown in Fig. 2). Fish images used, except Austrolebias charrua (taken by TJMVD), were modified from images attributed (from top to bottom) to Cisamarc (CC BY-SA 4.0), Cardet co6cs (CC BY-SA 3.0), J.C. Harf (CC BY-SA 3.0), Per Harald Olsen (CC BY 3.0) from Wikipedia and The Xiphophorus Genetic Stock Center, respectively.

Figure 2. State-dependent diversification rates and rates over time in Cyprinodontiformes.

Graphs on the left show net diversification rates over time for three clades in which annualism or viviparity evolved: (a) a clade of annual Rivulidae, (b) Goodeidae and (c) a clade of viviparous Poeciliidae (see stars in Fig. 1 and text for details). Coloured lines indicate net diversification rates against background rate (black lines), with shading around coloured lines representing 90% confidence intervals. On the right, state-dependent diversification rates extracted from BAMM analyses are shown for non-annual viviparous, annual oviparous and non-annual oviparous (NAO) clades. These graphs show the posterior distribution of rates for speciation (d), extinction (e) and net diversification (f), coloured by character state.