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.