Deceleration of morphological evolution in a cryptic species complex and its link to paleontological stasis.

José Cerca,Jana Wegbrod,Gunter Purschke,Dominik Siemon,Dave Stateczny,Torsten H. Struck,Christian Meyer,Dimitar Dimitrov

doi:10.1111/evo.13884

Abstract

Morphological stasis or the absence of morphological change is a well-known phenomenon in the paleontological record, yet it is poorly integrated with neontological evidence. Recent evidence suggests that cryptic species complexes may remain morphologically identical due to morphological stasis. Here, we describe a case of long-term stasis in the Stygocapitella cryptic species complex (Parergodrilidae, Orbiniida, Annelida). Using phylogenetic methods and morphological data, we find that rates of morphological evolution in Stygocapitella are significantly slower than in closely related taxa (Nerillidae, Orbiniidae). Assessment of quantitative and qualitative morphology revealed the presence of four morphotypes with only subtle differences, whereas molecular data supports 10 reproductively isolated clades. Notably, estimates for the time of Stygocapitella species divergence range from ∼275 million years to ∼18 million years, including one case of two morphologically similar species that have diverged about 140 million years ago. These findings provide evidence for morphological deceleration and long-term morphological stasis in Stygocapitella, and that speciation is not necessarily accompanied by morphological changes. The deceleration of morphological divergence in Stygocapitella can be potentially linked to niche conservatism and tracking, coupled with the fluctuating dynamics of the interstitial environment, or genetic constraints due to progenetic evolution. Finally, we conclude that failing to integrate speciation without morphological evolution in paleontology may bias estimates of rates of speciation and morphological evolution.

Highlights

The occurrence of morphological stasis, defined as little or no morphological evolution over extended periods of time, remains a controversial topic in evolutionary biology (Futuyma 2010)
DEMOGRAPHIC CHANGES AND ECOLOGICAL SEPARATION We focused on the Atlantic species for the analyses addressing potential ecological drivers of morphological stasis such as niche conservatism and/or the occurrence of fluctuating ecological dynamics (Sheldon 1996; Futuyma 2010; Lindholm 2014)
The Stygocapitella cryptic species complex is characterized by decelerated rates of morphological evolution and by long periods of morphological stasis

Summary

Introduction

The occurrence of morphological stasis, defined as little or no morphological evolution over extended periods of time, remains a controversial topic in evolutionary biology (Futuyma 2010). The postulation that morphological evolution occurs exclusively during speciation implies that adaptive and selective processes are insignificant during substantial parts of the evolutionary histories of species (e.g., Stanley 1975), challenging the accumulating evidence of the emerging “modern synthesis” (Futuyma 2005; Hunt and Rabosky 2014). The modern synthesis-punctuated equilibrium debate lasted for about two decades, over the years paleontological evidence was aligned with the major processes suggested by the modern synthesis: selection, drift, mutation, and gene flow (Hunt and Rabosky 2014). On the other hand, competing views have focused on developing theoretical frameworks underlying the deceleration of morphological evolution, which include scenarios of stabilizing selection (Charlesworth et al 1982; Hansen and Houle 2004; Futuyma 2010), niche conservatism and tracking (Futuyma 2010, 2015), fluctuating ecological conditions (Futuyma 1987, 2010, 2015; Sheldon 1996; Smith et al 2011), lack of new ecological interactions (Nordbotten and Stenseth 2016), constraints (Charlesworth et al 1982; Maynard Smith et al 1985; Wagner and Schwenk 2000; Hansen and Houle 2004; Futuyma 2010; Smith et al 2011), recurrent bottlenecks (Futuyma 2010), physiological or behavioral adaptation (Lee and Frost 2002; Futuyma 2010; Lassance et al 2019), and the influence of particular environments and environmental conditions (Westheide 1977; Futuyma 1987, 2010; Westheide and Rieger 1987; Giere 2009; Gueriau et al 2016)

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