Geographical ancestry of Lake Malawi's cichlid fish diversity.

Evolutionary biology rsbl.royalsocietypublishing.org Research Cite this article: Genner MJ, Ngatunga BP, Mzighani S, Smith A, Turner GF. 2015 Geographical ancestry of Lake Malawi’s cichlid fish diversity. Biol. Lett. 11: 20150232. http://dx.doi.org/10.1098/rsbl.2015.0232 Received: 26 March 2015 Accepted: 15 May 2015 Subject Areas: evolution, taxonomy and systematics Keywords: adaptive radiation, phylogeny, African fishes Author for correspondence: Martin J. Genner e-mail: Electronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2015.0232 or via http://rsbl.royalsocietypublishing.org. Geographical ancestry of Lake Malawi’s cichlid fish diversity Martin J. Genner1, Benjamin P. Ngatunga2, Semvua Mzighani2, Alan Smith3 and George F. Turner4 1 School of Biological Sciences, University of Bristol, Life Sciences Building, Bristol BS81TQ, UK Tanzania Fisheries Research Institute (TAFIRI), PO Box 9750, Dar-es-Salaam, Tanzania 3 School of Biological, Biomedical and Environmental Science, University of Hull, Hull HU67RX, UK 4 School of Biological Sciences, Bangor University, Bangor, Gwynedd LL572UW, UK 2 The Lake Malawi haplochromine cichlid flock is one of the largest vertebrate adaptive radiations. The geographical source of the radiation has been assumed to be rivers to the south and east of Lake Malawi, where extant representatives of the flock are now present. Here, we provide mitochondrial DNA evidence suggesting the sister taxon to the Lake Malawi radiation is within the Great Ruaha river in Tanzania, north of Lake Malawi. Estimates of the time of divergence between the Lake Malawi flock and this riverine sister taxon range from 2.13 to 6.76 Ma, prior to origins of the current radiation 1.20–4.06 Ma. These results are congruent with evaluations of 2–3.75 Ma fossil material that suggest past faunal connections between Lake Malawi and the Ruaha. We propose that ancestors of the Malawi radiation became isolated within the catchment during Pliocene rifting that formed both Lake Malawi and the Kipengere/Livingstone mountain range, before colonizing rivers to the south and east of the lake region and radiating within the lake basin. Identification of this sister taxon allows tests of whether standing genetic diversity has predisposed Lake Malawi cichlids to rapid speciation and adaptive radiation. 1. Introduction Adaptive radiations make up a high proportion of biodiversity. In many cases, ancestors or sister species of these flocks have been identified, as with Galapagos finches [1], Hawaiian silverswords [2] and Canadian three-spined sticklebacks [3]. Identification of their origins has enabled discussion of events that initiated adaptive radiation, and allowed tests of whether diversification has been promoted by novel mutations that have arisen since colonization, or instead whether adaptation is based primarily on pre-existing genetic variation [4]. This is an important issue to resolve, because it can explain why only some colonizing lineages radiate when provided with ecological opportunity, and how parallel adaptive radiation can take place rapidly in geographically separated habitats. The evolutionary origins of cichlid fishes radiations in East African lakes are largely elusive or speculative [5–8]. This is partly because of incomplete geographical and genomic sampling of riverine species within and surrounding lake basins. However, it is also due to intrinsic complexity of cichlid evolutionary relationships, as radiations may have been seeded by multiple riverine ancestors [8,9], and rivers can be recolonized by species with lacustrine ancestry [10]. A greater understanding of geographical and phylogenetic ancestry of cichlids is required to test whether functional genetic variation under divergent selection within lake radiations is present within riverine ancestors, and whether this variation has been shared among riverine cichlids through intraspecific gene flow and interspecific hybridization [9]. & 2015 The Author(s) Published by the Royal Society. All rights reserved. (a) (b) 1/93 1/99 Rufi ji Diplotaxodon, Pallidochromis 1/100 1/95 Rhamphochromis 1/80 Rukwa ‘Mbuna’, ‘deep benthic’, Astatotilapia calliptera 1/99 1/100 Ruaha vi Li 0.84/55 Copadichromis virginalis Astatotilapia calliptera, including Lake Chidya ng sto Astatotilapia sp. ‘Ruaha’ 0.99/72 ne Congo ng ra e 1/100 Lake Malawi 0.99/62 1/ 79 Lake Victoria region flock including A. ‘Blue Rufiji’ 1/100 Haplochromis gracilor Astatotilapia flaviijosephi Ruvuma 1/97 Astatotilapia burtoni 1/100 Astatotilapia desfontainii 1/100 Astatotilapia sp. Mindu Dam 0.93/92 1/94 Zambezi Haplochromis sp. (Congo) 1/100 ‘modern haplochromines’ Shi re 0.87/92 100 km Biol. Lett. 11: 20150232 Lu an gw a 1/97 0.88/55 Ruvuma Chilwa 1/100 Astatotilapia bloyeti (Kenya, AY930058) Astatotilapia sp. (Tanzania, AY930104) 1/ Astatotilapia bloyeti (Tanzania, EU753930) 96 Zambezi Astatotilapia tweddlei Rovuma 0.77/86 0.81/– Astatotilapia tweddlei Lake Chilwa 1/100 Tropheini (Lake Tanganyika) 1/100 1/100 0.99/ 81 Orthochromis stormsi Orthochromis polyacanthus Thoracochromis brauschi Serranochromis robustus Pseudocrenilabrus philander 1/99 Orthochromis kalungwishiensis Ctenochromis pectoralis 1/100 Astatoreochromis straeleni Astatoreochromis alluaudi Bathybates ferox 0.6 Tilapia sparrmanii Figure 1. (a) Lake Malawi and surrounding major river systems; (b) Bayesian phylogeny based on 544 mtDNA NADH2 sequences. Numbers above branches indicate posterior probabilities (black, values greater than 0.7 shown) and maximum-likelihood bootstrap support (blue, values greater than 70% shown). (Online version in colour.) Lake Malawi contains a radiating flock of at least 450 haplochromine species [11]. Early phylogenetic reconstructions suggested that the lake radiation was monophyletic [12,13]. More recent phylogenies show two species outside the Lake Malawi catchment also fall within the flock, namely Astatotilapia calliptera and Astatotilapia swynnertoni [5,8]. There have been indications that these are sister lineages to the radiating flock [5,8], but the hypothesis has not been well supported by either nuclear or mitochondrial DNA [5,8,14,15]. There is evidence that riverine representatives of the flock outside the catchment have seeded some lacustrine diversity in the radiation [8,16], but preceding this they may have escaped from Lake Malawi into neighbouring drainages. Given such uncertainty, and evidence of recent gene flow across catchment boundaries in A. calliptera [16], there is a need to further resolve relationships of Malawi endemics to cichlids in neighbouring drainages. To date, phylogenetic reconstructions have included haplochromines from many of the surrounding catchments (figure 1), including the Zambezi, Lake Chilwa, Ruvuma, Congo and Lake Rukwa catchments [5,8,13,17]. However, no published phylogenies have included haplochromines from (...truncated)