Teleostei: Percichthyidae: Gadopsis)Of South-Eastern Australia

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Teleostei: Percichthyidae: Gadopsis)Of South-Eastern Australia bs_bs_banner Biological Journal of the Linnean Society, 2014, ••, ••–••. With 6 figures A multigene molecular assessment of cryptic biodiversity in the iconic freshwater blackfishes (Teleostei: Percichthyidae: Gadopsis)of south-eastern Australia MICHAEL P. HAMMER1,2,3*, PETER J. UNMACK4,5, MARK ADAMS1,2, TARMO A. RAADIK6 and JERALD B. JOHNSON4 1Evolutionary Biology Unit, South Australian Museum, North Terrace, SA 5000, Australia 2Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Science, The University of Adelaide, Adelaide, SA 5005, Australia 3Curator of Fishes, Museum and Art Gallery of the Northern Territory, PO Box 4646, Darwin, NT 0801, Australia 4WIDB 401, Department of Biology, Brigham Young University, Provo, UT 84602, USA 5Institute for Applied Ecology and Collaborative Research Network for Murray-Darling Basin Futures, University of Canberra, Canberra, ACT 2601, Australia 6Aquatic Ecology Section, Arthur Rylah Institute for Environmental Research, Department of Environment and Primary Industries, 123 Brown Street, Heidelberg, VIC 3084, Australia Received 6 September 2013; revised 22 October 2013; accepted for publication 22 October 2013 Freshwater biodiversity is under ever increasing threat from human activities, and its conservation and manage- ment require a sound knowledge of species-level taxonomy. Cryptic biodiversity is a common feature for aquatic systems, particularly in Australia, where recent genetic assessments suggest that the actual number of freshwater fish species may be considerably higher than currently listed. The freshwater blackfishes (genus Gadopsis) are an iconic group in south-eastern Australia and, in combination with their broad, naturally divided distribution and biological attributes that might limit dispersal, as well as ongoing taxonomic uncertainty, they comprise an ideal study group for assessing cryptic biodiversity. We used a multigene molecular assessment including both nuclear (51 allozyme loci; two S7 introns) and matrilineal markers (cytb) to assess species boundaries and broad genetic substructure within freshwater blackfishes. Range-wide examination demonstrates the presence of at least six candidate species across two nominal taxa, Gadopsis marmoratus and Gadopsis bispinosus. Phylogeographical patterns often aligned to purported biogeographical provinces but occasionally reflected more restricted and unexpected relationships. We highlight key issues with taxonomy, conservation, and management for a species group in a highly modified region. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ••, ••–••. ADDITIONAL KEYWORDS: conservation – cryptic species – drainage divides – ESU – phylogeography – sea level changes. INTRODUCTION is generally reflected in the species richness and levels of endemism displayed for many organismal Australia is regarded as one of the world’s top 17 groups (Chapman, 2009). Among non-marine verte- megadiverse countries (Williams et al., 2001) and this brates, however, there is one glaring exception. Aus- tralia’s freshwater fish fauna has long been regarded *Corresponding author. E-mail: [email protected] as depauperate compared to those found in other © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ••, ••–•• 1 2 M. P. HAMMER ET AL. regions of comparable size and climate (Lundberg Gadopsis species are largely nocturnal and display et al., 2000; Allen, Midgley & Allen, 2003), such as cryptobenthic behaviour. An unusual combination of continental USA, which has over three times as many anatomical features led to early hypotheses of close described species (Page & Burr, 1991). Traditional relationships to various marine suborders such as explanations for this anomaly have invoked a range Blennioidei, Gadoidei, Ophidioidei, and Trachinoidei of climatic, topographic, and biogeographical factors (Ovenden, White & Sanger, 1988), until Johnson (Allen et al., 2003). However, an alternate explana- (1984) placed them in the family Percichthyidae. Sub- tion, originally proposed by Lundberg et al. (2000), sequent molecular work supported this hypothesis and more recently taken up by ourselves (Adams (Jerry, Eliphinstone & Baverstock, 2001; Near et al., et al., 2013; Hammer, Adams & Hughes, 2013a; 2012), with Gadopsis placed as the first branching Unmack, 2013), is that Australia’s low number of member of the family (Near et al., 2012). Their species also reflects the level of detailed taxonomic phylogenetic relationships within Percichthyidae effort devoted to this neglected group. In other words, imply an ancient history (early Tertiary or older). we hypothesize that the Australian freshwater fish The species-level taxonomic history of freshwater fauna is characterized by high levels of cryptic biodi- blackfishes has also been confounded, in this instance versity (sensu Beheregaray & Caccone, 2007). by limited, variable morphological characters for Although most of the obviously-distinctive mor- consistent discrimination. Gadopsis marmoratus photypic forms among the Australian freshwater was first described with the ambiguous type locality fishes have been described (Allen et al., 2003), there of ‘rivers in the southern parts of Australia’ have been few detailed assessments for a considerable (Richardson, 1848: 123). de Castelnau (1872) specu- number of species whose geographical distributions lated that there may be additional species in Victoria span multiple river basins and even major bio- and subsequently Gadopsis gracilis McCoy and geographical regions (Unmack, 2001, 2013). In Gadopsis gibbosus McCoy were recognized from the comparison, freshwater fishes displaying a similar Yarra and Bunyip rivers, respectively, followed by geographical pattern in the USA have typically been Gadopsis fuscus Steindachner from the ‘fresh- shown by detailed taxonomic investigation to contain waters of South Australia’. Thereafter, Ogilby (1913) cryptic species (Near & Benard, 2004; Berendzen, synonymized all these species under G. marmoratus. Olson & Barron, 2009; April et al., 2011). Supporting Parrish (1966) informally described Gadopsis this expectation, baseline molecular genetic studies tasmanica from Tasmania, which Sanger (1984) sub- have detected likely candidate species in a large pro- sequently determined to be conspecific with mainland portion of the geographically-widespread Australian populations of G. marmoratus. Finally, Sanger (1984) freshwater fish ‘species’ surveyed to date (Hammer described G. bispinosus on the basis of differences in et al., 2013a). dorsal spine counts and distinctive colour patterns, In the present study, we assess the generality of our resulting in the two-species taxonomic framework prediction that current species counts for the Austral- currently accepted (Allen et al., 2003; Hoese et al., ian freshwater fish fauna under-estimate the actual 2007). numbers by at least 50% (Hammer et al., 2013a; Nevertheless, taxonomic speculation continues Unmack, 2013) by exploring cryptic biodiversity in to plague Gadopsis on two fronts. First, other one of the more prominent groups, the freshwater undescribed forms have been suggested in the litera- blackfishes (genus Gadopsis). Two species are cur- ture. It has long been known that G. marmoratus rently recognized; the river blackfish Gadopsis from southern Victoria and Tasmania grow much marmoratus Richardson, which occurs in the exten- larger than those from the Murray-Darling Basin sive Murray-Darling Basin, and coastal systems from (Ogilby, 1913; Lintermans, 2007), and Parrish (1966) eastern Victoria to South Australia and northern and Sanger (1986) have recognized fish from western Tasmanian, and the two-spined blackfish Gadopsis Victoria as having lower dorsal spine counts. Second, bispinosus Sanger, which is limited to upland streams several studies have examined genetic variation using within the southern Murray-Darling Basin (Fig. 1). allozymes (Sanger, 1986; Ryan, Miller & Austin, Gadopsis marmoratus reaches a moderate size (i.e. 2004) and mitochondrial (mt)DNA variation (Ovenden 350–625 mm and approximately 5 kg) and, accord- et al., 1988; Waters, Lintermans & White, 1994; ingly, has greater recreational and cultural value Miller et al., 2004), all of which supported the distinc- for angling and eating (Lake, 1967; Jackson et al., tiveness of northern populations and, to some extent, 1996) than the smaller G. bispinosus (which grows to those in western Victoria. However, combined mor- approximately 350 mm; Lintermans, 2007). phological and molecular studies have been limited by Freshwater blackfishes are mysterious fish and a lack of comprehensive geographical coverage, which have proved to be an enigmatic group with regard has hindered interpretations and left unresolved the to both broader phylogentic affinities and taxonomy. status of all putative undescribed forms. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ••, ••–•• CRYPTIC BIODIVERSITY IN FRESHWATER BLACKFISHES 3 Figure 1. Locality data for all Gadopsis samples examined. For the corresponding site details, see Table 1. The shaded area identifies the known distribution of the two species currently recognized within Gadopsis. The symbol shape refers to the three deeper lineages identified, which represent ‘northern’ G. marmoratus (squares), ‘southern’ G. marmoratus (circles), and G. bispinosus (triangles), with the different shadings representing each candidate species. As a prominent inhabitant
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