Macroevolutionary Analyses Suggest That Environmental Factors, Not Venom Apparatus, Play Key Role in Terebridae Marine Snail Diversification.

Maria Vittoria Modica,Mandë Holford,Yves Terryn,Alexander E Fedosov,Nicolas Puillandre,Juliette Gorson,Gavin Malcolm,Jeanne Serb

doi:10.1093/sysbio/syz059

Abstract

How species diversification occurs remains an unanswered question in predatory marine invertebrates, such as sea snails of the family Terebridae. However, the anatomical disparity found throughput the Terebridae provides a unique perspective for investigating diversification patterns in venomous predators. In this study, a new dated molecular phylogeny of the Terebridae is used as a framework for investigating diversification of the family through time, and for testing the putative role of intrinsic and extrinsic traits, such as shell size, larval ecology, bathymetric distribution, and anatomical features of the venom apparatus, as drivers of terebrid species diversification. Macroevolutionary analysis revealed that when diversification rates do not vary across Terebridae clades, the whole family has been increasing its global diversification rate since 25 Ma. We recovered evidence for a concurrent increase in diversification of depth ranges, while shell size appeared to have undergone a fast divergence early in terebrid evolutionary history. Our data also confirm that planktotrophy is the ancestral larval ecology in terebrids, and evolutionary modeling highlighted that shell size is linked to larval ecology of the Terebridae, with species with long-living pelagic larvae tending to be larger and have a broader size range than lecithotrophic species. Although we recovered patterns of size and depth trait diversification through time and across clades, the presence or absence of a venom gland (VG) did not appear to have impacted Terebridae diversification. Terebrids have lost their venom apparatus several times and we confirm that the loss of a VG happened in phylogenetically clustered terminal taxa and that reversal is extremely unlikely. Our findings suggest that environmental factors, and not venom, have had more influence on terebrid evolution.

Highlights

Explaining the amazing biodiversity of species that inhabit our planet remains a significant challenge
Identifying the factors that influence predator-prey interactions and macroevolutionary patterns that lead to species diversification remains a challenge in neglected marine invertebrates
We examined the Terebridae, an understudied group of predatory sea snails that possess a notable range of foregut anatomical features and a complexity of venom arsenals comparable to other groups of the Conoidea

Summary

Introduction

Explaining the amazing biodiversity of species that inhabit our planet remains a significant challenge. With the exception of a few well-known taxa, such as vertebrates or angiosperms, current hypotheses about diversity patterns remain largely untested across the majority of Earth’s biodiversity (Jetz et al 2012; Pyron and Burbrink 2012; Rainford et al 2014; Legendre and Condamine 2018). This is especially true for marine invertebrates, in which their basic biology, diversification patterns, and evolutionary dynamics remain largely unknown. Environmental modifications may create new ecological opportunities for specific clades, through the availability of new habitats or the extinction of predators or competitors (Harmon et al 2008; Des Roches et al 2011; Parent and Crespi 2017)

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