Abstract

Among mammals, several lineages have independently adapted to a subterranean niche and possess similar phenotypic traits for burrowing (e.g., cylindrical bodies, short limbs, and absent pinnae). Previous research on mole-rats has revealed molecular adaptations for coping with reduced oxygen, elevated carbon dioxide, and the absence of light. In contrast, almost nothing is known regarding molecular adaptations in other subterranean lineages (e.g., true moles and golden moles). Therefore, the extent to which the recurrent phenotypic adaptations of divergent subterranean taxa have arisen via parallel routes of molecular evolution remains untested. To address these issues, we analyzed ∼8,000 loci in 15 representative subterranean taxa of four independent transitions to an underground niche for signatures of positive selection and convergent amino acid substitutions. Complementary analyses were performed in nonsubterranean “control” taxa to assess the biological significance of results. We found comparable numbers of positively selected genes in each of the four subterranean groups; however, correspondence in terms of gene identity between gene sets was low. Furthermore, we did not detect evidence of more convergent amino acids among subterranean species pairs compared with levels found between nonsubterranean controls. Comparisons with nonsubterranean taxa also revealed loci either under positive selection or with convergent substitutions, with similar functional enrichment (e.g., cell adhesion, immune response, and coagulation). Given the limited indication that positive selection and convergence occurred in the same loci, we conclude that selection may have acted on different loci across subterranean mammal lineages to produce similar phenotypes.

Highlights

  • IntroductionThe independent colonization of the same niche (e.g., marine, high-altitude, desert regions) by divergent mammalian lineages has led to pervasive and visible recurrent evolution of similar phenotypic traits (Uhen 2007; Schipper et al 2008; Kelley and Motani 2015)

  • The independent colonization of the same niche by divergent mammalian lineages has led to pervasive and visible recurrent evolution of similar phenotypic traits (Uhen 2007; Schipper et al 2008; Kelley and Motani 2015)

  • Tests performed on the ancestral branch of each clade revealed a total of 1,419 cases of positive selection, encompassing 1,267 positively selected genes (PSGs)

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Summary

Introduction

The independent colonization of the same niche (e.g., marine, high-altitude, desert regions) by divergent mammalian lineages has led to pervasive and visible recurrent evolution of similar phenotypic traits (Uhen 2007; Schipper et al 2008; Kelley and Motani 2015). High-throughput sequencing provides the means to perform comparative genome-wide screens of positive selection across taxa (Qiu et al 2012; Hendrickson 2013; Tsagkogeorga et al 2015). This expanding field of comparative genomics has revealed cases of parallel molecular adaptions associated with ecological specialization. High-altitude species living at low oxygen levels have been reported to show parallel molecular adaptations in hypoxia-resistance genes (Qiu et al 2012; Hendrickson 2013; Foll et al 2014). Recent studies have described parallel amino acid substitutions and positive selection in unrelated groups of marine mammals, which have evolved superficially similar body plans and face comparable demands for oxygen storage (Foote et al 2015; Zhou et al 2015). Despite the presence of shared substitutions in many loci, both of these studies concluded that there was limited evidence for widespread adaptive convergence related definitively to the aquatic niche

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