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Evolution Underground Molecular Phylogenetics and Evolution 50 (2009) 580–598 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Evolution underground: A molecular phylogenetic investigation of Australian burrowing freshwater crayfish (Decapoda: Parastacidae) with particular focus on Engaeus Erichson Mark B. Schultz a, Sarah A. Smith a, Pierre Horwitz b, Alastair M.M. Richardson c, Keith A. Crandall d, Christopher M. Austin e,* a Arafura Timor Research Facility, School of Environmental and Life Sciences, Charles Darwin University, PO Box 41775, Casuarina, NT 0811, Australia b School of Natural Sciences, Edith Cowan University, 100 Joondalup Drive, Joondalup, Perth, WA 6027, Australia c School of Zoology, University of Tasmania, Private Bag 5, Hobart, Tasmania 7001, Australia d Department of Biology, Brigham Young University, 675 Widstoe Building, Provo, UT 84602-5181, USA e School of Environmental and Life Sciences, Charles Darwin University, Darwin, NT 0909, Australia article info abstract Article history: Phylogenetic relationships and species boundaries of Australian burrowing freshwater crayfish belonging Received 7 August 2008 to the genera Engaeus, Engaewa, Geocharax, Gramastacus and Tenuibranchiurus are investigated using Revised 26 November 2008 combined mitochondrial and nuclear DNA sequence data and Bayesian and Maximum Parsimony meth- Accepted 28 November 2008 ods. Phylogenies are statistically compared to previously published hypotheses. Engaeus, Engaewa, Geo- Available online 11 December 2008 charax, Gramastacus and Tenuibranchiurus form a strongly supported monophyletic clade. This grouping is independently supported by morphology but unites geographically highly disjunct lineages. Our data Keywords: show two cryptic species in Geocharax, one cryptic species in Gramastacus and two cryptic species within Phylogenetics the highly divergent Engaeus lyelli lineage. Using a Bayesian relaxed molecular clock method, the 16S Biogeography Evolution rDNA data show generic-level diversification coinciding with the transition from a wet to arid palaeocli- Relaxed molecular clock mate near the mid Miocene. Burrowing freshwater crayfish Ó 2008 Elsevier Inc. All rights reserved. Mitochondrial ribosomal Nuclear protein-coding DNA 16S GAPDH Systematics Australia 1. Introduction continents. Reciprocal monophyly of the northern and southern hemisphere superfamilies—the Astacoidea Latreille, 1802 and the Freshwater crayfish are found on every continent except conti- Parastacoidea Huxley, 1878, respectively—support this model nental Africa, the Indian sub-continent and Antarctica (Crandall (Crandall and Buhay, 2008; Porter et al., 2005; Sinclair et al., 2004). and Buhay, 2008). The consensus of geographical, morphological, The Parastacoidea contains one family, the Parastacidae Huxley, molecular and palaeontological evidence strongly supports their 1878, and has its centre of species diversity in southeastern Austra- monophyletic origin from marine ancestors (e.g. Crandall et al., lia where eight of the 10 currently recognised extant Australian 2000; Scholtz, 1993; Sinclair et al., 2004; Tsang et al., 2008) some- genera are found. Four additional genera are scattered about the time around 280 million years ago (Ma) (Porter et al., 2005). Fresh- southern hemisphere with two in southern South America, one water crayfish then dispersed throughout the Pangean in Madagascar and one in New Zealand. Crayfish body and trace supercontinent before it divided (185 Ma) into the Laurasian fossils (burrows) confirm a Parastacid presence in southeastern (northern hemisphere) and Gondwanan (southern hemisphere) Australia since at least 106–116 million years (m.y.) before the present (Martin et al., 2008). The distribution of extant Parastaci- dae remains consistent with ancient Gondwanan connections and * Corresponding author. Fax: +61 (0)8 8946 6700. fossils pre-date complete separation of Australia from Antarctica E-mail addresses: [email protected] (M.B. Schultz), sarah.smith@cdu. (Bedatou et al., 2008; Crandall and Buhay, 2008; Martin et al., edu.au (S.A. Smith), [email protected] (P. Horwitz), alastair.richardson@utas. edu.au (A.M.M. Richardson), [email protected] (K.A. Crandall), chris.austin 2008; Sampson et al., 1998; Veevers, 2006). Many forms of evi- @cdu.edu.au, [email protected] (C.M. Austin). dence corroborate southeastern Australia as an important area 1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2008.11.025 M.B. Schultz et al. / Molecular Phylogenetics and Evolution 50 (2009) 580–598 581 for freshwater crayfish evolution. Based on a phylogenetic assess- If they were indeed more closely related to one another than they ment, Whiting et al. (2000) recommended southeastern Australia are to other taxa, then assessments of divergence times between (including Tasmania) as a priority region for the conservation of the genera Engaeus, Engaewa, Geocharax, Gramastacus and Tenui- freshwater crayfish. branchiurus would enable a better understanding of the evolution- Since the 19th century, various conflicting evolutionary scenar- ary context of their successful adaptive radiation. ios for the Parastacidae have been assembled from morphological, Of the 10 extant Australian genera, comprising approximately geographical and/or palaeontological data (e.g. Huxley, 1880; Ort- 150 species (e.g. Austin and Ryan, 2002; Coughran, 2005a,b; Crand- mann, 1902; Riek, 1959, 1969, 1972; Rode and Babcock, 2003). all et al., 1999; Hansen and Richardson, 2006; Horwitz, 1990a, More recently, molecular data have been used, sometimes in com- 1994a; Horwitz and Adams, 2000; Morgan, 1997), Euastacus (49 bination with morphological and ecological data, to address ques- species), Cherax (42 species) and Engaeus (35 species) hold the tions of relationships between the Australian genera or between most species diversity, with Engaeus being comparatively the least the Australian and New Zealand genera (e.g. Austin, 1995; Crandall studied using nucleotide data. Despite this, some key taxonomic et al., 1999, 1995; Patak and Baldwin, 1984; Patak et al., 1989; studies of Engaeus have been performed, using electrophoretic, Schultz et al., 2007). From these studies, it is evident that many as- morphological and nucleotide data, which have revealed uncer- pects of the phylogeny of the Australian Parastacidae remain un- tainties in the relationships within and between species of Engaeus clear. These uncertainties require resolution before a proper (Horwitz, 1990a; Horwitz et al., 1990; Schultz et al., 2007). For understanding of evolutionary diversification within the Parastac- example, preliminary mitochondrial 16S rDNA data suggest that idae can be achieved. Engaeus lyelli (Clark, 1936) is highly divergent from the other Enga- A conspicuous feature of Australian Parastacidae is their ecolog- eus species and may in fact represent a new genus (Schultz et al., ical and morphological diversity. This principally relates to some 2007). This suggestion is not, in itself, entirely new, as nearly every genera having successfully radiated into semipermanent aquatic author who has dealt with the taxonomy of E. lyelli has disagreed environments, evolving a largely underground lifestyle and an abil- with regard to its designation (Clark, 1936; Horwitz, 1990a; Kane, ity to construct large and often complex burrow systems (Horwitz, 1964; Riek, 1969). Such findings still await a full treatment of Enga- 1985; Horwitz and Richardson, 1986). Adaptation to burrowing eus and phylogenetic analysis with the addition of nuclear nucleo- has resulted in the evolution of unique or distinctive morphologi- tide data. cal features, such as the reduction of the size and width of the Engaeus has a relatively restricted distribution, occurring abdomen (Hobbs, 1974; Horwitz, 1988b, 1990a; Horwitz and Rich- throughout the northern part of the island of Tasmania and the ardson, 1986; Suter, 1977a,b) and vertically or sub-vertically in- southeastern Australian mainland region. The geographical density clined great chelae (the first pereopod) (Riek, 1969, 1972). of species in this genus is very high (Horwitz, 1990a), even in com- Based on orientation of the great chelae and burrowing habits, parison to the more widespread and species-rich genera Cherax Riek (1972) denoted two divisions within Parastacidae: the moder- (e.g. see Riek, 1969) and Euastacus (e.g. see Morgan, 1997). The ate burrowers, which hold the great chelae and move the fingers in habitats of Engaeus species have endured geological shifts (Hor- a horizontal or oblique plane, and the strong burrowers, which witz, 1988a; Lambeck and Chappell, 2001; Schultz et al., 2008) hold the great chelae and move the fingers in a vertical or sub-ver- and contemporary anthropogenic impacts (e.g. see Ierodiaconou tical plane. Within the Australian genera, Riek (1972) classified et al., 2005; Horwitz, 1990b, 1994b, 1995)—the latter providing moderate burrowers as Astacopsis Huxley, 1878, Euastacus Clark, conservation challenges. 1936, Cherax Erichson, 1846, Parastacoides (Erichson, 1846) (now From a conservational perspective, greater than 21% of known Ombrastacoides Hansen and Richardson, 2006 and Spinastacoides parastacid species (38 of 177 recognised species) are already listed Hansen and Richardson, 2006), Geocharax Clark, 1936 and Gramas- as vulnerable, endangered or critically endangered and fourteen of tacus Riek, 1972. He proposed that these genera
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