Phylogeny and Phylogeography of Altolamprologus: Ancient Introgression and Recent Divergence in a Rock-Dwelling Lake Tanganyika Cichlid Genus
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Hydrobiologia DOI 10.1007/s10750-016-2896-2 ADVANCES IN CICHLID RESEARCH II Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus Stephan Koblmu¨ller . Bruno Nevado . Lawrence Makasa . Maarten Van Steenberge . Maarten P. M. Vanhove . Erik Verheyen . Christian Sturmbauer . Kristina M. Sefc Received: 22 February 2016 / Revised: 17 June 2016 / Accepted: 19 June 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Stenotopic specialization to a fragmented divergence among genetic clades. Low rates of habitat promotes the evolution of genetic structure. It dispersal, perhaps along gastropod shell beds that is not yet clear whether small-scale population struc- connect patches of rocky habitat, and periodic sec- ture generally translates into large-scale intraspecific ondary contact during lake level fluctuations are divergence. In the present survey of mitochondrial apparently sufficient to maintain genetic connectivity genetic structure in the Lake Tanganyika endemic within each of the two Altolamprologus species. The Altolamprologus (Teleostei, Cichlidae), a rock-dwell- picture of genetic cohesion was interrupted by a single ing cichlid genus comprising A. compressiceps and A. highly divergent haplotype clade in A. compressiceps calvus, habitat-induced population fragmentation con- restricted to the northern part of the lake. Comparisons trasts with weak phylogeographic structure and recent between mitochondrial and nuclear phylogenetic reconstructions suggested that the divergent mito- chondrial clade originated from ancient interspecific Electronic supplementary material The online version of this article (doi:10.1007/s10750-016-2896-2) contains supple- introgression. Finally, ‘isolation-with-migration’ mentary material, which is available to authorized users. models indicated that divergence between the two Altolamprologus species was recent (67–142 KYA) Guest editors: S. Koblmu¨ller, R. C. Albertson, M. J. Genner, and proceeded with little if any gene flow. As in other K. M. Sefc & T. Takahashi / Advances in Cichlid Research II: Behavior, Ecology and Evolutionary Biology rock-dwelling cichlids, recent population expansions S. Koblmu¨ller (&) Á M. Van Steenberge Á L. Makasa C. Sturmbauer Á K. M. Sefc Lake Tanganyika Research Unit, Department of Fisheries, Institute of Zoology, University of Graz, Universita¨tsplatz Ministry of Fisheries and Livestock, 2, 8010 Graz, Austria P. O. Box 420055, Mpulungu, Zambia e-mail: [email protected] M. Van Steenberge Á M. P. M. Vanhove B. Nevado Á M. Van Steenberge Á E. Verheyen Laboratory of Biodiversity and Evolutionary Genomics, Operational Directorate Taxonomy and Phylogeny, Royal Department of Biology, University of Leuven, Charles Belgian Institute of Natural Sciences, Vautierstraat 29, Debe´riotstraat 32, 3000 Louvain, Belgium 1000 Brussels, Belgium M. Van Steenberge Á M. P. M. Vanhove Present Address: Biology Department, Royal Museum for Central Africa, B. Nevado Leuvensesteenweg 13, 3080 Tervuren, Belgium Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK 123 Hydrobiologia were inferred in both Altolamprologus species, which the open-water habitat contain virtually no barriers to may be connected with drastic lake level fluctuations. dispersal, and cichlid species specialized to these habitats show little if any population genetic structure Keywords Cichlidae Á Mitochondrial replacement Á at all (Shaw et al., 2000; Taylor & Verheyen, 2001; Phylogeography Á Lake level fluctuations Á Pereyra et al., 2004; Genner et al., 2008, 2010a; Lamprologini Á Hybridization Anseeuw et al., 2011; Koblmu¨ller et al., 2015a). The majority of studies addressing the genetic structure of cichlid species in the two lakes did so by Introduction sampling populations within a small portion of the species’ entire distribution range (see references The genetic structure within a species is often above). It is not yet clear whether findings regarding predicted by components of the species’ ecology and small-scale population structure can be extrapolated to life history traits (Wiens & Donoghue, 2004). For large-scale phylogeographic patterns. Significant instance, generalist species and species with good genetic differentiation can evolve among fragmented dispersal abilities tend to show little phylogeographic populations within relatively short periods of time. structure (e.g. Cadena et al., 2011; Koblmu¨ller et al., However, large-scale phylogeographic patterns have 2012; Diedericks & Daniels, 2014), whereas species been shown to be influenced by the long-term history that are specialized to particular, fragmented habitats of the species, including range shifts and introgression or food sources are often divided into distinct popu- among differentiated lineages during secondary con- lations and develop marked phylogeographic patterns tact in the course of lake level fluctuations (Verheyen (e.g. Young et al., 1996; Row et al., 2010; Kajtoch et al., 1996; Sturmbauer et al., 2001; Egger et al., et al., 2014). This contrast is particularly evident when 2007; Nevado et al., 2009). Therefore, distinct pop- the different species occur in the same region. In the ulation genetic structure may, but need not, go along two East African lakes Malawi and Tanganyika, with a clear-cut phylogeographic pattern; and vice stenotopic cichlid species inhabiting the discontinuous versa, species with high levels of gene flow across the rocky littoral consistently show remarkable genetic geographical scale of previous population genetic population differentiation, even across very short studies may still be genetically structured on a larger geographic distances (e.g. van Oppen et al., 1997; scale. Markert et al., 1999; Taylor et al., 2001; Rico & Due to logistic and sometimes political reasons, Turner, 2002; Pereyra et al., 2004; Duftner et al., 2006; lake-wide sampling in Lakes Malawi and Tanganyika Koblmu¨ller et al., 2011; Sefc et al., 2007; Wagner & can be difficult, and only few species have been McCune, 2009; Nevado et al., 2013; Van Steenberge investigated throughout large parts of their distribu- et al., 2015; Sefc et al., 2016). Differentiation is lower tion ranges. The stenotopic rock-dwelling genus and only occurs on a larger geographic scale in less Tropheus from Lake Tanganyika is one example in specialized species and species that inhabit the which both population genetic and lake-wide phylo- intermediate habitat, i.e. the transition between rocky geographic studies have been conducted. In this fish, and sandy habitat surrounding the rocky habitat strong small-scale population differentiation contrasts patches (Koblmu¨ller et al., 2007a, 2009; Sefc et al., with evidence for ancient introgression among phylo- 2007; Kotrschal et al., 2012). Finally, the sandy and genetically old lineages (Sturmbauer et al., 2005; Sefc et al., 2007; Egger et al., 2007; Koblmu¨ller et al., 2011; Sefc et al., 2016). A similar picture—deep intraspeci- M. P. M. Vanhove fic divergences and past introgression among geo- Department of Botany and Zoology, Faculty of Science, graphically distant populations—emerged in a Masaryk University, Kotla´rˇska´ 2, 611 37 Brno, Czech Republic phylogeographic study of another rock-dwelling cich- lid of Lake Tanganyika, the Neolamprologus bri- M. P. M. Vanhove chardi/pulcher complex (Duftner et al., 2007). In Capacities for Biodiversity and Sustainable Development, contrast, two species that are less strictly restricted to Operational Directorate Natural Environment, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, rocky habitat (Lamprologus callipterus and Neolam- 1000 Brussels, Belgium prologus fasciatus) exhibit clear phylogeographic 123 Hydrobiologia structure but shallower intraspecific divergence (Ne- variation in colour pattern (Kohda et al., 1996; vado et al., 2009), and a highly mobile benthopelagic Konings, 1998), and comparisons among three popu- species (Boulengerochromis microlepis) shows no lations in the very south of Lake Tanganyika detected phylogeographic structure on a lake-wide scale and significant population genetic and morphometric dif- very shallow intraspecific divergence (Koblmu¨ller ferentiation in A. compressiceps (Spreitzer et al., et al., 2015a). Similarly, in Lake Malawi, the pelagic 2012), a pattern potentially indicating pronounced species Diplotaxodon limnothrissa shows no phylo- levels of lake-wide phylogeographic structuring. Fur- geographic structure on a lake-wide scale (Shaw et al., thermore, if habitat preferences correlate with phylo- 2000). geographic structure, we expect to see a similar Here, we investigate the phylogeographic structure phylogeographic pattern in Altolamprologus as in the in two closely related species of the Lake Tanganyika rock-dwellers Tropheus spp. and N. pulcher/brichardi, cichlid genus Altolamprologus, a member of the with ancient introgression among deeply divergent ‘ossified group’ within the tribe Lamprologini (Sti- genetic lineages (Sturmbauer et al., 2005; Duftner assny, 1997). The genus diverged from its sister group et al., 2007; Egger et al., 2007). In this study, we use [1 MYA (Sturmbauer et al., 2010) and includes only mitochondrial and nuclear sequence data to uncover two described species, Altolamprologus compressi- the phylogeographic structure and demographic his- ceps and A. calvus. A. compressiceps has a lake-wide tory of A. calvus and A. compressiceps,