Discovering the silk road: Nuclear and mitochondrial sequence data resolve the phylogenetic relationships among theraphosid spider subfamilies

Highlights

• A first molecular phylogeny for theraphosid spiders is presented.

• Monophyly of many subfamilies is supported, however the subfamily of Schismatothelinae appeared to be paraphyletic.

• We found evidence for validity of the Poecilotheriinae and Stromatopelminae.

• Obtained data leads to identification of sound biogeographical clades in theraphosid spiders.

• We compare our molecular- with morphology based phylogenies.

Abstract

The mygalomorph spiders in the family Theraphosidae, also known as “tarantulas”, are one of the most popular and diverse groups of arachnids, but their evolutionary history remains poorly understood because morphological analyses have only provided mostly controversial results, and a broad molecular perspective has been lacking until now. In this study we provide a preliminary molecular phylogenetic hypothesis of relationships among theraphosid subfamilies, based on 3.5 kbp of three nuclear and three mitochondrial markers, for 52 taxa representing 10 of the 11 commonly accepted subfamilies. Our analysis confirms the monophyly of the Theraphosidae and of most recognized theraphosid subfamilies, supports the validity of the Stromatopelminae and Poecilotheriinae, and indicates paraphyly of the Schismatothelinae. The placement of representatives of Schismatothelinae also indicates possible non-monophyly of Aviculariinae and supports the distinction of the previously contentious subfamily Psalmopoeinae. Major clades typically corresponded to taxa occurring in the same biogeographic region, with two of them each occurring in Africa, South America and Asia. Because relationships among these major clades were poorly supported, more extensive molecular data sets are required to test the hypothesis of independent colonization and multiple dispersal events among these continents.

Introduction

The family Theraphosidae, commonly referred to as “tarantulas”, are a group of mygalomorph spiders which includes some of the largest arachnids on earth. Tarantulas are among the most prominent spiders, widely known to the general public as horror movie performers and also commonly kept as pets (e.g. Klaas, 1989). Given this distinguished position among spiders, it is striking that their deep phylogeny and higher classification remain unstudied from a molecular perspective. The Theraphosidae contain 962 nominal species (World Spider Catalogue, 2017), and most authors accept 11 theraphosid subfamilies (Kambas, 2017) occurring on all continents except Antarctica (West et al., 2008) (Table 1). This diversity is also reflected in different ecological adaptations and natural histories. The group includes arboreal, terrestrial and cave dwelling taxa. Different theraphosid species display a variety of defensive mechanisms such as stridulation, venomous bite or urticating setae (Marshall et al., 1995, Bertani and Guadanucci, 2013). Furthermore, considering their wide range of distribution and their presumably poor dispersal capacity, theraphosids represent good models for biogeographic research.

As is commonplace in arachnological taxonomy (Coddington, 2005, Ramirez, 2014), the systematics of theraphosid spiders is largely based on analysis of morphological characters. Using those, Raven (1985) formulated a first evolutionary hypothesis on intrafamilial relationships, but later recognized the limits of this morphology-based approach by referring to Theraphosidae as a “taxonomic nightmare” (Raven, 1990). Subsequent revisions of theraphosid subfamilies and genera continued using mostly or only morphological characters (e.g. Smith, 1990, Pérez-Miles et al., 1996, Bertani, 2000, Gallon, 2003, Gallon, 2005a, West et al., 2008, West et al., 2012, West and Nunn, 2010, Guadanucci, 2011a, Guadanucci, 2011b, Guadanucci, 2014, Fukushima and Bertani, 2017), but other studies have shown that many traditional morphological characters of spiders can be affected by a high degree of homoplasy (Platnick and Gertsch, 1976, Goloboff, 1993, Bond and Opell, 2002, Hedin and Bond, 2006, Ayoub et al., 2007, Bond et al., 2012). Within Theraphosidae, the poorly defined subfamily Ischnocolinae comprises several taxa of uncertain taxonomical status and has been found to be paraphyletic (Raven, 1985). Several ischnocoline genera show an unresolved phylogenetic position, e.g. Nesiergus, which has been removed from Ischnocolinae (sensu strictu) by Guadanucci (2014) but not given an alternative (therefore herein referred to the Ischnocolinae sensu lato). Besides the Ischnocolinae conundrum, the monophyly and validity of several other subfamilies are also under discussion. Particularly, this regards the Selenocosmiinae (West and Nunn, 2010), Aviculariinae (West et al., 2008, Fukushima and Bertani, 2017) and Eumenophorinae (Guadanucci, 2011a, Guadanucci, 2011b, Mirza et al., 2014), as well as the validity of Poecilotheriinae (Schmidt, 1995, West et al., 2008, West et al., 2012) and Psalmopoeinae (Samm and Schmidt, 2010).

Comparative molecular studies on theraphosids thus far are limited to the species to genus level, for instance in Aphonopelma (Hamilton et al., 2011, Hamilton et al., 2016), Brachypelma (Longhorn et al., 2007, Mendoza and Francke, 2017), Grammostola (Montes De Oca et al., 2015) and Bonnetina (Ortiz and Francke, 2016), whereas phylogenetic relationships among genera and subfamilies remain significantly understudied from a molecular perspective, with few exceptions (e.g., Turner et al., 2017). Several recent studies comprehensively addressed the phylogeny of spiders in general (e.g. Fernandez et al., 2014, Wheeler et al., 2016, Garrison et al., 2016), including representatives of the Theraphosidae but not addressing the phylogeny within the family.

In this study, our goal is to provide a first molecular hypothesis on the broadest scale of theraphosid evolutionary history, i.e., on the relationships among major clades at the subfamily level, serving as a baseline to direct future in-depth studies. We discuss our phylogeny in terms of genus to subfamily level classification. Furthermore, we examine the geographic distribution of major clades identified.