Adaptive divergence in shell morphology in an ongoing gastropod radiation from Lake Malawi

Bert Van Bocxlaer,Xavier Vekemans,Pieter R Gurdebeke,Claudia M Ortiz-Sepulveda

doi:10.1186/s12862-019-1570-5

Abstract

BackgroundEcological speciation is a prominent mechanism of diversification but in many evolutionary radiations, particularly in invertebrates, it remains unclear whether supposedly critical ecological traits drove or facilitated diversification. As a result, we lack accurate knowledge on the drivers of diversification for most evolutionary radiations along the tree of life. Freshwater mollusks present an enigmatic example: Putatively adaptive radiations are being described in various families, typically from long-lived lakes, whereas other taxa represent celebrated model systems in the study of ecophenotypic plasticity. Here we examine determinants of shell-shape variation in three nominal species of an ongoing ampullariid radiation in the Malawi Basin (Lanistes nyassanus, L. solidus and Lanistes sp. (ovum-like)) with a common garden experiment and semi-landmark morphometrics.ResultsWe found significant differences in survival and fecundity among these species in contrasting habitats. Morphological differences observed in the wild persisted in our experiments for L. nyassanus versus L. solidus and L. sp. (ovum-like), but differences between L. solidus and L. sp. (ovum-like) disappeared and re-emerged in the F1 and F2 generations, respectively. These results indicate that plasticity occurred, but that it is not solely responsible for the observed differences. Our experiments provide the first unambiguous evidence for genetic divergence in shell morphology in an ongoing freshwater gastropod radiation in association with marked fitness differences among species under controlled habitat conditions.ConclusionsOur results indicate that differences in shell morphology among Lanistes species occupying different habitats have an adaptive value. These results also facilitate an accurate reinterpretation of morphological variation in fossil Lanistes radiations, and thus macroevolutionary dynamics. Finally, our work testifies that the shells of freshwater gastropods may retain signatures of adaptation at low taxonomic levels, beyond representing an evolutionary novelty responsible for much of the diversity and disparity in mollusks altogether.

Highlights

Ecological speciation is a prominent mechanism of diversification but in many evolutionary radiations, in invertebrates, it remains unclear whether supposedly critical ecological traits drove or facilitated diversification
For many evolutionary radiations across the tree of life accurate knowledge is still lacking on the drivers of diversification and how disparity in organismal traits among distant lineages and diversity at a low taxonomic level are related
An example is the polemic on ecophenotypic plasticity versus adaptive punctuated change associated with speciation in the fossil freshwater mollusks of the Turkana Basin [23,24,25,26,27,28]

Summary

Introduction

Ecological speciation is a prominent mechanism of diversification but in many evolutionary radiations, in invertebrates, it remains unclear whether supposedly critical ecological traits drove or facilitated diversification. For many evolutionary radiations across the tree of life accurate knowledge is still lacking on the drivers of diversification and how disparity in organismal traits among distant lineages and diversity at a low taxonomic level are related. Most experimental work has focused on genetic and environmental determinants of shell shape and color [11,12,13,14,15], on how the presence or absence of predators affects life-history traits [16] and shell shape [17,18,19], and on the ecological context of invasion success in clonal freshwater snails [20, 21] Many of these studies report phenotypic plasticity to be commonplace, but a strong taxonomic bias prevails, especially in freshwater gastropods [22]. In the absence of a detailed insight into ecophenotypic plasticity, we cannot accurately discern intraspecific and interspecific variation, which hampers an accurate interpretation of morphological change in both extant and fossil species lineages

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Conclusion