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Phylogeny and Historical Biogeography of Ancient Assassin Spiders (Araneae: Archaeidae) in the Australian Mesic Zone: Evidence F

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Phylogeny and Historical Biogeography of Ancient Assassin Spiders (Araneae: Archaeidae) in the Australian Mesic Zone: Evidence F Molecular Phylogenetics and Evolution 62 (2012) 375–396 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny and historical biogeography of ancient assassin spiders (Araneae: Archaeidae) in the Australian mesic zone: Evidence for Miocene speciation within Tertiary refugia ⇑ Michael G. Rix a, , Mark S. Harvey a,b,c,d a Department of Terrestrial Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC, Perth, Western Australia 6986, Australia b School of Animal Biology, University of Western Australia, 35 Stirling Highway, Crawley, Perth, Western Australia 6009, Australia c Division of Invertebrate Zoology, American Museum of Natural History, New York, NY 10024, USA d California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA 94118, USA article info abstract Article history: The rainforests, wet sclerophyll forests and temperate heathlands of the Australian mesic zone are home Received 28 July 2011 to a diverse and highly endemic biota, including numerous old endemic lineages restricted to refugial, Revised 11 October 2011 mesic biomes. A growing number of phylogeographic studies have attempted to explain the origins Accepted 13 October 2011 and diversification of the Australian mesic zone biota, in order to test and better understand the mode Available online 21 October 2011 and tempo of historical speciation within Australia. Assassin spiders (family Archaeidae) are a lineage of iconic araneomorph spiders, characterised by their antiquity, remarkable morphology and relictual Keywords: biogeography on the southern continents. The Australian assassin spider fauna is characterised by a high Arachnida diversity of allopatric species, many of which are restricted to individual mountains or montane systems, Palpimanoidea Araneomorphae and all of which are closely tied to mesic and/or refugial habitats in the east and extreme south-west of Systematics mainland Australia. We tested the phylogeny and vicariant biogeography of the Australian Archaeidae Rainforest (genus Austrarchaea Forster & Platnick), using a multi-locus molecular approach. Fragments from six Short-range endemism mitochondrial genes (COI, COII, tRNA-K, tRNA-D, ATP8, ATP6) and one nuclear protein-coding gene (His- Great Dividing Range tone H3) were used to infer phylogenetic relationships and to explore the phylogeographic origins of the diverse Australian fauna. Bayesian analyses of the complete molecular dataset, along with differentially- partitioned Bayesian and parsimony analyses of a smaller concatenated dataset, revealed the presence of three major Australian lineages, each with non-overlapping distributions in north-eastern Queensland, mid-eastern Australia and southern Australia, respectively. Divergence date estimation using mitochon- drial data and a rate-calibrated relaxed molecular clock revealed that major lineages diverged in the early Tertiary period, prior to the final rifting of Australia from East Antarctica. Subsequent speciation occurred during the Miocene (23–5.3 million years ago), with tropical and subtropical taxa diverging in the early- mid Miocene, prior to southern and temperate taxa in the mid-late Miocene. Area cladograms reconciled with Bayesian chronograms for all known Archaeidae in southern and south-eastern Australia revealed seven potentially vicariant biogeographic barriers in eastern Queensland, New South Wales and southern Australia, each proposed and discussed in relation to other mesic zone taxa. Five of these barriers were inferred as being of early Miocene age, and implicated in the initial vicariant separation of endemic regio- nal clades. Phylogeographic results for Australian Archaeidae are congruent with a model of sequential allopatric speciation in Tertiary refugia, as driven by the contraction and fragmentation of Australia’s mesic biomes during the Miocene. Assassin spiders clearly offer great potential for further testing histor- ical biogeographic processes in temperate and eastern Australia, and are a useful group for better under- standing the biology and biogeography of the Australian mesic zone. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction 1996; Crisp et al., 2004) and a more recent climatic history domi- nated by widespread and ongoing aridification (Crisp et al., 2004; The island continent of Australia is an ancient, dynamic land- Byrne et al., 2008). The Australian biota is thus a mixture of relic- scape, with a temperate Gondwanan heritage (Hopper et al., tual mesic elements, later colonisers and more recently evolved arid-adapted taxa (Crisp et al., 2004), the latter having diversified ⇑ Corresponding author. Fax: +61 8 9212 3882. spectacularly since the mid-Miocene (Byrne et al., 2008). E-mail address: [email protected] (M.G. Rix). Australia’s remaining ‘mesic biomes’ are broadly restricted to the 1055-7903/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2011.10.009 376 M.G. Rix, M.S. Harvey / Molecular Phylogenetics and Evolution 62 (2012) 375–396 continent’s southern, eastern and tropical northern coastlines ies are required to complement and test prevailing biogeographic (Crisp et al., 2004; Ponniah and Hughes, 2004; Byrne et al., 2008) hypotheses born out of recent research on birds, reptiles and and are largely concordant with the distribution of rainforests amphibians. and closed and tall open forests in Australia’s east and extreme The assassin spiders of the family Archaeidae (Fig. 1) are an south-west (see Specht, 1981; Webb and Tracey, 1981; Adam, ancient and iconic lineage of araneomorph spiders, remarkable 1992). These refugial, mesic habitats, despite having undergone for their extraordinary appearance, highly specialised ecology, evo- enormous contractions since the Miocene, are home to a significant lutionary antiquity and endemism on the southern continents proportion of Australia’s biodiversity (Webb and Tracey, 1981; (Forster and Platnick, 1984; Harvey, 2002a; Wood et al., 2007; Yeates et al., 2002) and include a highly endemic biota (e.g. Schnei- Wood, 2008; Rix and Harvey, 2011). Assassin spiders are obligate der et al., 1998; Webb and Tracey, 1981; Moritz et al., 2000; Rix predators of other spiders, and all possess a modified, grossly- et al., 2009; Bell et al., 2010; Cooper et al., 2011; Hugall and Stani- elevated cephalothorax and ‘head’ region bearing long, spear-like sic, 2011). Rigorous molecular phylogenetic studies are critical to chelicerae (Fig. 1), used to hunt and capture their spider prey testing biogeographic hypotheses and understanding alternative (Legendre, 1961; Forster and Platnick, 1984; Wood et al., 2007; patterns of speciation and divergence in a complex Australian con- Wood, 2008; Rix and Harvey, 2011). This highly specialised araneo- text (Crisp et al., 2004) and a growing number of phylogeographic phagic morphology is unique among arachnids, making the studies have attempted to explain the origins and diversification of Archaeidae among the most instantly-recognisable of all spider the Australian mesic zone biota, for both vertebrates (e.g. Cracraft, families. They are the icon of Madagascar’s rich spider fauna 1991; Joseph and Moritz, 1994; Joseph et al., 1993, 1995; Schnei- (Griswold, 2003; Wood, 2008), and while long considered among der et al., 1998; Schneider and Moritz, 1999; Schäuble and Moritz, the rarest and most enigmatic of spiders (Forster and Platnick, 2001; Hoskin et al., 2003; Jennings et al., 2003; O’Connor and 1984), recent dedicated research in South Africa, Madagascar and Moritz, 2003; Knowles et al., 2004; Chapple et al., 2005; Moussalli Australia has revealed diverse and highly endemic faunas in all et al., 2005; Couper et al., 2008; Hugall et al., 2008; Colgan et al., three countries, each of considerable evolutionary and biogeo- 2009; Bell et al., 2010) and invertebrates (e.g. Ward, 1980; Hugall graphic significance (Platnick, 1991a, 1991b; Lotz, 1996, 2003, et al., 2003; Sota et al., 2005; Ponniah and Hughes, 2004, 2006; 2006; Harvey, 2002a; Wood et al., 2007; Wood, 2008; Rix and Baker et al., 2008; Schultz et al., 2009; Hugall and Stanisic, 2011; Harvey, 2011). Lucky, 2011; Cooper et al., 2011). Many of these invertebrate stud- The history of the discovery and documentation of living and ies have focused on relatively few insect, mollusc and crustacean fossil assassin spiders highlights the great antiquity of the taxa (e.g. ants, snails and freshwater crayfish), and additional stud- family, and points to the utility of the Archaeidae for testing Fig. 1. Australian assassin spiders (family Archaeidae). (A-B) Habitus images of live specimens: (A) juvenile Austrarchaea raveni Rix and Harvey, 2011 from Mount Glorious, Queensland; (B) female Austrarchaea sp. nov. (WA-4) from Karri Valley, Western Australia. (C–G) Lateral carapace profiles of male Austrarchaea spp., showing variation in the height of the carapace and length of the ‘neck’: (C) Austrarchaea sp. nov. (VIC-2) from Acheron Gap, Victoria; (D) Austrarchaea sp. nov. (WA-1) from Mount Hassell, Western Australia; (E) A. christopheri Rix and Harvey, 2011 from Dorrigo National Park, New South Wales; (F) A. nodosa (Forster, 1956) from Lamington National Park, south-eastern Queensland; (G) Austrarchaea sp. nov. from Mount Elliot, north-eastern Queensland. Image (A) by Greg Anderson, used with permission; image (B) by M. Rix. M.G. Rix, M.S. Harvey / Molecular Phylogenetics and Evolution 62 (2012) 375–396 377 historical
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