KEYWORDS: adaptive landscape, niche dynamics, morphological parallelism, comparative phylogenetic methods, supertree, chronogram, phylogram.
1 | INTRODUCTION
Convergent evolution, the independent evolution of similar phenotypes, has long fascinated biologists because it represents natural replicates of the evolutionary process (Darwin, 1859; McGhee, 2011). It is traditionally seen as straightforward evidence of adaptation to similar environmental pressures (Mayr, 2013; Simpson, 1953), yet recent studies have highlighted other contributing factors and encouraged a more nuanced view (Conway Morris, 2010; Losos, 2011; Stayton, 2015). Firstly, the important role of evolutionary constraints has been emphasized (Conway Morris, 2010; McGhee, 2011). Without constraints on the adaptive landscape of an organism, the same niches need never arise, and even when they do, lineages may evolve different traits to overcome the same niche-specific function (Losos, 2011). Furthermore, when constraints are strong enough, morphological convergence may occur for reasons other than adaptation to environmental pressures, or simply by chance (Losos, 2011; Stayton, 2008). Understanding the drivers of morphological convergence in a group therefore requires not only identification of the phenomenon itself, but further investigation into its relationship with behavior and niche-space. Such broad, combined analyses of morphology and behavior in turn provide insights into the evolutionary dynamics, functional morphology, and life history of the study group, as demonstrated in recent analyses on birds (Pigot et al., 2020), mammals (Sansalone et al., 2020), and marine tetrapods (Kelley & Motani, 2015), yet equivalent studies on invertebrates are few (Ceccarelli et al., 2019).
The spider infraorder Mygalomorphae, often called ‘primitive spiders’, currently contains 31 families of relatively large, robust spiders that generally live sedentary lives in permanent retreats or burrows (Bond et al., 2012; Opatova et al., 2020; Raven, 1985). It includes species commonly known as tarantulas, trapdoor spiders, and funnel-web spiders. The group has a tumultuous taxonomic history, but the first major work, bringing some order to the chaos, was that of Raven (1985). This exhaustive morphological review, and the accompanying cladistics-based phylogeny, served as the foundation of mygalomorph systematics for two decades and remains the most complete synopsis of mygalomorph morphology available. However, the implementation of molecular methods has revealed phylogenetic relationships in stark discordance with those deduced from morphology: over half the traditional families were revealed to be paraphyletic and accepted interfamilial relationships have changed dramatically (Bond et al., 2012; Hedin et al., 2018, 2019; Hedin & Bond, 2006; Montes de Oca et al., 2022; Opatova et al., 2020). With the recent taxon-rich, genomic phylogeny of Opatova et al. (2020), accepted mygalomorph relationships have largely stabilized. What is still required, however, is a reconciliation of mygalomorph morphology and behavior with this new phylogeny, to understand the broad evolutionary patterns in the group that were previously obscured by taxonomic and phylogenetic uncertainty and instability.
One pattern that is often proposed to explain the discordance between morphological and molecular hypotheses of mygalomorph relationships is convergence in somatic morphology associated with life history characteristics (Hedin et al., 2019; Hedin & Bond, 2006; Opatova et al., 2020). The retreats of these spiders come in a diversity of forms including, among many others: funnel-like silken retreats built in crevices with extensive capture webs; burrows in the ground with or without a trapdoor entrance; and short nests constructed against tree trunks (Coyle, 1986). Reconstructions of these ‘behavioral niches’ on new molecular phylogenies have consistently found that each has evolved several times across mygalomorphs (Hedin et al., 2019; Opatova et al., 2020). Intuitive associations between particular niches and somatic characters have long been recognized, for example, between elongate posterior lateral spinnerets and the construction of capture webs (Chamberlin & Ivie, 1945; Eskov & Zonshtein, 1990) and between strong lateral ‘digging spines’ on the anterior legs and the construction of burrows (Goloboff, 1993; Raven, 1985). However, to date neither the overarching influence of convergence on mygalomorph morphology, nor specific patterns of correlation with behavior of any morphological feature, have ever been specifically tested.
The aim of this study is to characterize what is potentially a major evolutionary trend in the Mygalomorphae – the adaptive convergence of somatic morphology in correlation with the behavioral niches inhabited by the group. Using a selection of recent, robust genomic phylogenies available in the literature, we construct a genus-level phylogram and chronogram, and a taxon-rich supertree. Next, we score all genera in these trees for a discrete dataset of two behavioral and 55 somatic-morphological characters. We then perform the most detailed reconstruction of behavioral niche in the Mygalomorphae to date, to understand patterns of convergence in behavioral niche and the association between retreat type and retreat-entrance type. Next, to compare the influence of behavioral niche and evolutionary history on general somatic morphology we perform non-metric multidimensional scaling on the full morphological dataset, visualizing somatic variation in morpho-space. Finally, we test for correlation between a subset of morphological features and particular behavioral niches to shed light on the function of these features and the drivers of adaptive convergence in the Mygalomorphae.