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Nocturnal Claroteine Catfishes Reveal Dual Colonisation but a Single Molecular Phylogenetics and Evolution 73 (2014) 119–128 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Nocturnal claroteine catfishes reveal dual colonisation but a single radiation in Lake Tanganyika ⇑ Claire R. Peart a,b, , Roger Bills c, Mark Wilkinson b, Julia J. Day a a Department of Genetics, Evolution & Environment, University College London, Gower Street, London WC1E 6BT, UK b Department of Life Sciences, The Natural History Museum, Cromwell Road, South Kensington, London SW7 5BD, UK c South African Institute for Aquatic Biodiversity, Private Bag 1015, 6140 Grahamstown, South Africa article info abstract Article history: Lake Tanganyika (LT) is a biodiversity hotspot supporting many endemic radiations that provide compar- Received 23 May 2013 ative systems in which to investigate if there are common factors leading to the build-up of its consid- Revised 3 December 2013 erable diversity. Despite LT containing the highest diversity of lacustrine catfishes on Earth, the Accepted 17 January 2014 evolutionary relationships of nocturnal catfishes within the sub-family Claroteinae have not been inves- Available online 3 February 2014 tigated and it is unknown if its constituent genera have diversified via single or independent colonisation events. We report the first molecular phylogeny of the LT claroteine catfishes based on a multigene data- Keywords: set (three nuclear markers, two mitochondrial totalling 4227 bp), including 85 samples from LT and out- Siluriformes side of the lake basin. These data support LT claroteine monophyly, with the exclusion of the LT endemic Africa Lake Tanganyika Chrysichthys brachynema that independently colonised the lake but has not radiated. Multiple sampling Diversification localities from LT and the use of Bayesian species delimitation methods reveal additional locally Species delimitation restricted diversity within the LT Claroteinae clade. Fossil calibrated molecular divergence dates suggest that diversification occurred within full lake conditions as demonstrated in other LT lineages. Ó 2014 Elsevier Inc. All rights reserved. 1. Introduction sification and the presence of sexual selection are associated with diversification but lake surface area is not. This suggests that radi- Insular faunas are widely considered to be particularly well sui- ations may be predictable to some extent in terms of propensity to ted to studies assessing which factors generate and maintain diver- diversify if not necessarily in terms of exact outcomes. For exam- sity (e.g. MacArthur and Wilson, 1967; Wallace, 1880). The great ple, whilst there are repeated phenotypes between the East African lakes of East Africa’s Rift Valley represent a system of freshwater Rift Lakes (Fryer and Iles, 1972), smaller cichlid radiations in crater ‘islands’ and as a result have attracted much attention, not least be- lakes (611 species) that are similar in size to other non-cichlid Rift cause of their hyper-diverse, endemic cichlid fish radiations and Lake radiations, do not show equivalent species assemblages interest in the possible mechanisms responsible for generating this (Schliewen et al., 1994). spectacular diversity (e.g., Day et al., 2008; Genner and Turner, An alternative way to determine if there are common factors 2012; Haesler and Seehausen, 2005; Muschick et al., 2012). Addi- facilitating the generation of biological diversity is to investigate tionally, Lake Malawi and Lake Tanganyika host a number of inde- the similarities and differences between radiations in divergent pendent radiations facilitating the search for general patterns and taxa within the same environment. Among the East African Rift causes. Lakes, Lake Tanganyika (LT) offers a uniquely broad diversity of dif- One approach to identifying common patterns across multiple ferent-sized endemic radiations from independent lineages with radiations is to look at the same or closely related taxa in different differing ecologies and life histories e.g., gastropods (approxi- environments. For example, Wagner et al. (2012) investigated cich- mately 70 species, West and Michel, 2000), copepods (68 species lid colonisation and diversification in lakes throughout Africa and and sub-species, Coulter, 1991), Mastacembelus eels (14 species, found that deep lakes, high net solar radiation, more time for diver- Brown et al., 2010, 2011), Synodontis catfishes (11 species, Day and Wilkinson, 2006; Day et al., 2009; Wright and Page, 2006), Platythelphusa crabs (nine species, Marijnissen et al., 2006), Tan- ⇑ Corresponding author at: Department of Genetics, Evolution & Environment, ganikallabes catfishes (three species, Wright and Bailey, 2012). University College London, Gower Street, London WC1E 6BT, UK. Cichlid fishes may not be representative of other taxa due to their E-mail addresses: [email protected] (C.R. Peart), [email protected] (R. Bills), [email protected] (M. Wilkinson), [email protected] (J.J. Day). exceptional ability to speciate. Thus, comparative data from other http://dx.doi.org/10.1016/j.ympev.2014.01.013 1055-7903/Ó 2014 Elsevier Inc. All rights reserved. 120 C.R. Peart et al. / Molecular Phylogenetics and Evolution 73 (2014) 119–128 radiations are important in testing whether patterns of diversifica- colonise and diversify simultaneously, indicating a common exter- tion in cichlids are also seen across a range of other lineages. nal driver of diversification? Additionally we test whether the A further advantage of LT as a study system is its long history as overall diversity of claroteine catfishes is currently underestimated a water body and relative stability allowing increased time for col- by using sampling from around the lake and employing Bayesian onisation and diversification. Lake Tanganyika is the oldest of the species delimitation to assess if the observed morphological diver- East African Lakes at 9–12 Ma (Cohen et al., 1993) and has expe- sity in Phyllonemus corresponds to increased species diversity. Fi- rienced periods of low lake levels that led to the separation of dif- nally, the phylogeny is used to determine if the traditional ferent basins (Cohen et al., 1997) but has not fully dried out, unlike taxonomy of the group is supported, or whether there is any sup- Lakes Malawi and Victoria. port for the alternative taxonomy of Mo (1991). In order to compare radiations, age estimates for each clade are required. Recent methodological advances in the construction of 2. Methods species trees using multispecies coalescence offer the possibility of improved estimation of speciation times for recently diverged 2.1. Sampling taxa taking into account genetic divergence prior to speciation (Drummond et al., 2012; McCormack et al., 2011). In addition The specimens included in this study were collected using a molecular species delimitation offers an objective way to define variety of methods e.g., scuba, snorkelling, fyke nets, rotenone the evolutionarily significant units used in analyses based on mul- and obtained in local fish markets. The majority of specimens are tiple loci ensuring that equivalent taxonomic units are compared, preserved as vouchers; a full list of the taxa in this study is given which will also facilitate future comparison with other radiations. in Supplementary materials. Samples were collected from both the northern and southern basins within LT from Burundi, Tanza- 1.1. The study system nia and Zambia. Complete sampling of LT is, however, problematic in light of the large portion of LT in the Democratic Republic of the Catfishes of the sub-family Claroteinae from LT offer a useful Congo and its ongoing political instability. system to study lacustrine diversification due to the inclusion of In total 85 specimens are included in this study, representing 10 multiple genera, encompassing widespread and locally restricted of the 15 described LT claroteine species (and additional specimens species that occur at different depths (Hardman, 2008), as well not identified to species level) and four putative new Phyllonemus as rocky shore and deep water specialists. Four claroteine genera species. An additional 21 claroteine specimens from outside LT were have representatives in LT. Three genera are endemic: the mono- included expanding the sampling to include 5 of the 8 claroteine typic genus Bathybagrus (Bailey and Stewart, 1984), Lophiobagrus genera. The following claroteine genera are not included in this (four species; Bailey and Stewart, 1984) and Phyllonemus. Within study: Amarginops (single species), Gephyroglanis (three species) Phyllonemus there are three currently described species, (Risch, and Pardiglanis (single species). Many Chrysichthys specimens in 1987), although morphological variation is suggestive of additional museum collections are not identified to species level because they species (Bills, pers. obs.). The fourth genus, Chrysichthys, is wide- are often difficult to assign based on morphological features, so sam- spread throughout Africa, with seven species currently described ples were chosen to maximise geographic coverage in an attempt to in LT (Hardman, 2008), and a further 40 elsewhere (Eschmeyer, maximise genetic diversity. The species Rheoglanis dendrophorus is 2013). There is some controversy over the taxonomy of the group not included here, although it has been used in a previous study dat- with Mo (1991) expanding the genus Bathybagrus and reassigning ing divergences involving the Claroteidae (Lundberg et al., 2007). some
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