Radula diversification promotes ecomorph divergence in an adaptive radiation of freshwater snails

Abstract

24Adaptive diversification of complex traits plays a pivotal role for the evolution of organismal 25 diversity. However, the underlying molecular mechanisms remain largely elusive. In the 26 freshwater snail genus Tylomelania, adaptive radiations were likely promoted by trophic 27 specialization via diversification of their key foraging organ, the radula. To investigate the 28 molecular basis of radula diversification and its contribution to lineage divergence, we use 29 pooled tissue-specific transcriptomes of two sympatric Tylomelania sarasinorum ecomorphs. 30We show that divergence in both gene expression and coding sequences is stronger between 31 radula transcriptomes compared to mantle and foot transcriptomes. These findings support the 32 hypothesis that diversifying selection on the radula is driving speciation in Tylomelania 33 radiations. We also identify several candidate genes for radula divergence. Putative homologs 34 of some candidates (hh, arx, gbb) also contributed to trophic specialization in cichlids and 35Darwin's finches, indicating that some molecular pathways may be especially prone to adaptive 36 diversification. 3Main 38 Adaptive radiations provide extreme examples of rapid phenotypic and ecological 39 diversification and therefore feature prominently among model systems for adaptation and 40 speciation 1-6 . In many adaptive radiations, lineage divergence is promoted by diversification of 41 a few traits, like foraging organs, which acted as key adaptive traits in several radiations 3,7-13 . 42Understanding the genetic bases of key adaptive traits is essential because they shape 43 evolutionary trajectories of diversifying lineages 14,15 . Although previous findings are likely 44 biased towards few genes of large effect 2,16 , they also indicate that polygenic selection [17][18][19] , 45 adaptive introgression 20-24 , and regulatory evolution 18,21,25,26 promote diversification in adaptive 46 radiations [17][18][19] . However, much remains to be discovered about the genetic basis of adaptive 47 traits, the molecular evolution underlying their diversification, and their contribution to 48 speciation 2,27 . Particularly, our understanding of gene expression divergence and its 49 contribution to speciation is still in its infancy 28,29 . Here we investigate the genetic basis of 50 diversification of the molluscan key foraging organ (the radula) and its role for lineage 51 divergence in a radiation of freshwater snails, using two sympatric ecomorphs of Tylomelania 52 sarasinorum 30 . 53The genus Tylomelania is endemic to the central Indonesian island Sulawesi and underwent 54 several radiations following colonizations of different lake systems 31,32 . Lacustrine species 55 flocks occur across heterogeneous substrates and exhibit remarkable radula diversity ( Figure 56 1) 33,34 . In contrast, riverine clades occupy relatively homogenous substrates, have uniformly 57 shaped radular teeth and include comparatively few species 33,34 . Additionally, similar radula 58 morphologies likely ...