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Did Hypertrophied Lips Evolve Once Or Repeatedly in Lake Malawi Cichlid Fishes? C Erschienen in: BMC Evolutionary Biology ; 18 (2018). - 179 http://dx.doi.org/10.1186/s12862-018-1296-9 Darrin Hulsey et al. BMC Evolutionary Biology (2018) 18:179 https://doi.org/10.1186/s12862-018-1296-9 RESEARCH ARTICLE Open Access Phylogenomics of a putatively convergent novelty: did hypertrophied lips evolve once or repeatedly in Lake Malawi cichlid fishes? C. Darrin Hulsey1* , Jimmy Zheng2, Roi Holzman3, Michael E. Alfaro2, Melisa Olave1 and Axel Meyer1 Abstract Background: Phylogenies provide critical information about convergence during adaptive radiation. To test whether there have been multiple origins of a distinctive trophic phenotype in one of the most rapidly radiating groups known, we used ultra-conserved elements (UCEs) to examine the evolutionary affinities of Lake Malawi cichlids lineages exhibiting greatly hypertrophied lips. Results: The hypertrophied lip cichlids Cheilochromis euchilus, Eclectochromis ornatus, Placidochromis “Mbenji fatlip”, and Placidochromis milomo areallnestedwithinthenon-mbunacladeofMalawi cichlids based on both concatenated sequence and single nucleotide polymorphism (SNP) inferred phylogenies. Lichnochromis acuticeps that exhibits slightly hypertrophied lips also appears to have evolutionary affinities to this group. However, Chilotilapia rhoadesii that lacks hypertrophied lips was recovered as nested within the species Cheilochromis euchilus. Species tree reconstructions and analyses of introgression provided largely ambiguous patterns of Malawi cichlid evolution. Conclusions: Contrary to mitochondrial DNA phylogenies, bifurcating trees based on our 1024 UCE loci supported close affinities of Lake Malawi lineages with hypertrophied lips. However, incomplete lineage sorting in Malawi tends to render these inferences more tenuous. Phylogenomic analyses will continue to provide powerful inferences about whether phenotypic novelties arose once or multiple times during adaptive radiation. Keywords: Adaptive radiation, East African Rift Lakes, Fatlips, Phylogenomics Background these adaptively radiating groups exceptionally difficult Phylogenies are critical to testing convergence. Evolu- [17–23]. However, phylogenomic analyses could allow us tionary trees can provide the framework for determining to determine whether traits such as the elongate bodies of whether similar phenotypes have multiple origins or piscivores, distinctive color patterns of fish inhabiting whether these traits have arisen only a single time [1–6]. rocky reefs, or even bizarre phenotypes like greatly hyper- Molecular phylogenies of East African cichlids provided trophied lips have arisen multiple times in radiations like some of the first examples of using DNA sequence data the Lake Malawi cichlids. to establish the repeated evolution of similar phenotypes Hypertrophied, or greatly enlarged, lips have arisen in radiations inhabiting different lakes [7–10]. Yet, clarify- several times independently across fish diversity. Line- ing whether cichlid lineages have evolved traits conver- ages possessing hypertrophied lips are present in the gently within particular cichlid radiations that inhabit the sailfin silverside fishes from the Malili lakes of Sulawesi same lake has remained problematic [11–16]. Addition- [24] as well as in the barb species inhabiting Lake Tana ally, the short periods (< 2 mya) over which cichlid groups of Ethiopia [25, 26]. But the best-known group that ex- like those inhabiting Lake Victoria and Lake Malawi have hibits hypertrophied lips are the cichlid fishes (Fig. 1). diversified have made reconstructing the phylogenies of Cichlids exhibiting greatly hypertrophied lips have inde- pendently arisen in the Nicaraguan crater lakes, large South American rivers, Lake Tanganyika, Lake Victoria, * Correspondence: [email protected] – 1Department of Biology, University of Konstanz, Konstanz, Germany and Lake Malawi [10, 27 33]. This phenotype is often Full list of author information is available at the end of the article associated with feeding from rocky surfaces, and is likely © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-2-124q68x21hwh35 Darrin Hulsey et al. BMC Evolutionary Biology (2018) 18:179 Page 2 of 13 Fig. 1 Convergent evolution of hypertrophied lip phenotypes in cichlids fishes. This phenotype has arisen independently in a number of cichlid lineages inhabiting regions ranging from the Nicaraguan Rift Lakes (Amphilophus labiatus), South America (Crenicichla tendybaguassu), Lake Tanganyika (Lobochilotes labiatus), Lake Victoria (Haplochromis chilotes), and Lake Malawi (Cheilochromis euchilus, Eclectochromis ornatus, Placidochromis “Mbenji fatlip”, and Placidochromis milomo). The lineages containing hypertrophied lips from these disparate geographic settings outside of Lake Malawi are well established as phylogenetically independent [79]. However, it is unclear if the hypertrophied lip phenotype has arisen convergently multiple times or alternatively only once within Lake Malawi exceptionally effective for sucking prey from difficult- sequence markers have known limitations for phyl- to-access cracks and crevices [32, 34, 35]. The presence ogeny reconstruction [17, 18] and body pigmentation could of hypertrophied lips could also form the basis of mate often be a poor predictor of evolutionary affinities [31, 50]. choice and ultimately speciation [36]. However, there is Next-generation sequence based phylogenomic ap- substantial plasticity in the size of the lips depending on proaches have the potential to greatly clarify evolution- the substrates individuals use during feeding, so the ary patterns. For instance, sequence capture of large hypertrophied lip phenotype might be readily gained and numbers of highly conserved regions of organismal lost during evolution [37]. genomes shared among evolutionary distant taxa, or The repeated evolution of hypertrophied lips across ultra-conserved elements (UCEs), has been efficiently both a diversity of teleosts as well as its presence within used to generate massive genomic data sets capable of numerous phylogenetically disparate cichlid lineages sug- resolving relationships at deep timeframes [51–56]. gests that the hypertrophied lip lineages in Lake Malawi Additionally, one of the most compelling characteristics could have evolved convergently. With approximately of UCEs for phylogenetic reconstruction is that the 1000 species of haplochromine cichlids, the opportunity flanking regions increase in variant sites as the distance for the repeated origin of adaptive traits within the Malawi from the UCE center increases, thereby potentially radiation is extensive [38–40]. Also, Malawi species with allowing for resolution of nodes at more recent evolu- hypertrophied lips are currently classified into several dif- tionary timescales [13, 57, 58]. Yet, even with the ability ferent genera based in part on their extensive differences to generate these massive datasets, the best approach to in body pigment patterns [27, 41–44]. For instance, the analyzing this type of sequence data in rapid radiations species Cheilochromis euchilus exhibits black horizontal like Lake Malawi is largely unclear [13, 59, 60]. In Lake stripes while Placidochromis milomo has vertical barred Malawi cichlids, single loci of from 500 to 1000 base pigmentation that could indicate affinities with evolution- pairs that are often used for phylogenetic reconstruc- arily disparate Malawi clades (Fig. 1). Additionally, the tion could frequently have only a few variable single Malawi hypertrophied lip species Placidochromis milomo nucleotide polymorphisms (SNPs) [23]. This lack of vari- has been inferred, based on mitochondrial DNA, to be ation could make evolutionary inferences problematic. Fur- phylogenetically nested within the rock-dwelling “mbuna” thermore, interspecific gene flow could be common in this clade (Fig. 2) while other species with hypertrophied lips largely sympatric radiation [17, 47, 49, 61] providing oppor- have been inferred to lie within the largely sand-dwelling, tunities for extensive recombination during this group’sdi- or non-mbuna, group of Malawi cichlids [22, 45–49]. vergence among even the few SNPs that do exist in a single However, phylogenies reconstructed using mitochondrial sequence. Because of the vagaries of molecular evolution, Darrin Hulsey et al. BMC Evolutionary Biology (2018) 18:179 Page 3 of 13 relationships differently than if hybridization was more common between hypertrophied lip species and other members of the Malawi cichlid radiation. We used both sequence data and single nucleotide polymorphisms (SNPs) generated from genotyping a large number of UCE loci to infer the relationships among several lineages within Lake Malawi. First, we examined whether there was greater evidence for extensive para- phyly or alternatively monophyly of several lineages of Lake Malawi’s hypertrophied lip
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