Abstract

Key changes in ecological niche space are often critical to understanding how lineages diversify during adaptive radiations. However, the converse, or understanding why some lineages are depauperate and relictual, is more challenging, as many factors may constrain niche evolution. In the case of the insect order Grylloblattodea, highly conserved thermal breadth is assumed to be closely tied to their relictual status, but has not been formerly tested. Here, we investigate whether evolutionary constraints in the physiological tolerance of temperature can help explain relictualism in this lineage. Using a comparative transcriptomics approach, we investigate gene expression following acute heat and cold stress across members of Grylloblattodea and their sister group, Mantophasmatodea. We additionally examine patterns of protein evolution, to identify candidate genes of positive selection. We demonstrate that cold specialization in Grylloblattodea has been accompanied by the loss of the inducible heat shock response under both acute heat and cold stress. Additionally, there is widespread evidence of selection on protein‐coding genes consistent with evolutionary constraints due to cold specialization. This includes positive selection on genes involved in trehalose transport, metabolic function, mitochondrial function, oxygen reduction, oxidative stress, and protein synthesis. These patterns of molecular adaptation suggest that Grylloblattodea have undergone evolutionary trade‐offs to survive in cold habitats and should be considered highly vulnerable to climate change. Finally, our transcriptomic data provide a robust backbone phylogeny for generic relationships within Grylloblattodea and Mantophasmatodea. Major phylogenetic splits in each group relate to arid conditions driving biogeographical patterns, with support for a sister‐group relationship between North American Grylloblatta and Altai‐Sayan Grylloblattella, and a range disjunction in Namibia splitting major clades within Mantophasmatodea.

Highlights

  • Species that are considered relicts are by definition old, taxonomically depauperate lineages, where extinction has substantially diminished their former diversity (Grandcolas, Nattier, & Trewick, 2014; Habel, Assmann, Schmitt, & Avise, 2010)

  • In order to generate a reliable dataset for phylogenetic analysis, we identified orthologous genes that were shared across our study taxa

  • Previous research has shown that thermal breadth and critical thermal limits do not vary in North American species (Schoville et al, 2015), consistent with constraints on thermal niche evolution

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Summary

| INTRODUCTION

Species that are considered relicts are by definition old, taxonomically depauperate lineages, where extinction has substantially diminished their former diversity (Grandcolas, Nattier, & Trewick, 2014; Habel, Assmann, Schmitt, & Avise, 2010). We examine genomic divergence patterns for evidence of positive selection in protein-coding genes related to cold specialization These data provide an opportunity to resolve uncertainty in the deeper phylogeny of Grylloblattodea (Jarvis & Whiting, 2006; Schoville, Uchifune, & Machida, 2013), in the sister-group relationship among Asian and North American genera. Grylloblattodea and Mantophasmatodea diverged more than 150 million years ago (Eberhard, Schoville, & Klass, 2018; Misof et al, 2014), and, despite this long period of evolutionary history, they remain the two smallest insect orders (33 and 25 currently described extant species, respectively) Both lineages had formerly widespread fossil ancestors, and, as a result, they are both considered relictual orders (Roth et al, 2014; Schoville & Kim, 2011). We focus on the evolutionary consequences of relictualism in Grylloblattodea, to closely examine the role of niche evolution in this climate specialized lineage

| MATERIALS AND METHODS
Findings
| DISCUSSION
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