The evolutionary history of Xiphophorus fish and their sexually selected sword: a genome‐wide approach using restriction site‐associated DNA sequencing
Abstract
Next‐generation sequencing (NGS) techniques are now key tools in the detection of population genomic and gene expression differences in a large array of organisms. However, so far few studies have utilized such data for phylogenetic estimations. Here, we use NGS data obtained from genome‐wide restriction site‐associated DNA (RAD) (∼66000 SNPs) to estimate the phylogenetic relationships among all 26 species of swordtail and platyfish (genus Xiphophorus) from Central America. Past studies, both sequence and morphology‐based, have differed in their inferences of the evolutionary relationships within this genus, particularly at the species‐level and among monophyletic groupings. We show that using a large number of markers throughout the genome, we are able to infer the phylogenetic relationships with unparalleled resolution for this genus. The relationships among all three major clades and species within each of them are highly resolved and consistent under maximum likelihood, Bayesian inference and maximum parsimony. However, we also highlight the current cautions with this data type and analyses. This genus exhibits a particularly interesting evolutionary history where at least two species may have arisen through hybridization events. Here, we are able to infer the paternal lineages of these putative hybrid species. Using the RAD‐marker‐based tree we reconstruct the evolutionary history of the sexually selected sword trait and show that it may have been present in the common ancestor of the genus. Together our results highlight the outstanding capacity that RAD sequencing data has for resolving previously problematic phylogenetic relationships, particularly among relatively closely related species.
Number of times cited: 53
- Zachary W. Culumber and Michael Tobler, Correlated evolution of thermal niches and functional physiology in tropical freshwater fishes, Journal of Evolutionary Biology, 31, 5, (722-734), (2018).
- Julian R Dupuis, Christianne M Mcdonald, John H Acorn and Felix A H Sperling, Genomics-informed species delimitation to support morphological identification of anglewing butterflies (Lepidoptera: Nymphalidae: Polygonia), Zoological Journal of the Linnean Society, 10.1093/zoolinnean/zlx081, 183, 2, (372-389), (2017).
- Zhi‐Yao Ma, Jun Wen, Jing‐Pu Tian, Abbas Jamal, Long‐Qing Chen and Xiu‐Qun Liu, Testing reticulate evolution of four Vitis species from East Asia using restriction‐site associated DNA sequencing, Journal of Systematics and Evolution, 56, 4, (331-339), (2018).
- Natascha Dorothea Wagner, Susanne Gramlich and Elvira Hörandl, RAD sequencing resolved phylogenetic relationships in European shrub willows (Salix L. subg. Chamaetia and subg. Vetrix) and revealed multiple evolution of dwarf shrubs, Ecology and Evolution, 8, 16, (8243-8255), (2018).
- Mercedes Burns, James Starrett, Shahan Derkarabetian, Casey H. Richart, Allan Cabrero and Marshal Hedin, Comparative performance of double‐digest RAD sequencing across divergent arachnid lineages, Molecular Ecology Resources, 17, 3, (418-430), (2016).
- Josephine R. Paris, Jamie R. Stevens, Julian M. Catchen and Susan Johnston, Lost in parameter space: a road map for stacks, Methods in Ecology and Evolution, 8, 10, (1360-1373), (2017).
- Paolo Franchini, Daniel Monné Parera, Andreas F. Kautt and Axel Meyer, quaddRAD: a new high‐multiplexing and PCR duplicate removal ddRAD protocol produces novel evolutionary insights in a nonradiating cichlid lineage, Molecular Ecology, 26, 10, (2783-2795), (2017).
- J.R. Dupuis, B.M.T. Brunet, H.M. Bird, L.M. Lumley, G. Fagua, B. Boyle, R. Levesque, M. Cusson, J.A. Powell and F.A.H. Sperling, Genome-wide SNPs resolve phylogenetic relationships in the North American spruce budworm ( Choristoneura fumiferana ) species complex, Molecular Phylogenetics and Evolution, 10.1016/j.ympev.2017.04.001, 111, (158-168), (2017).
- Yong Suk Chung, Sang Chul Choi, Tae-Hwan Jun and Changsoo Kim, Genotyping-by-sequencing: a promising tool for plant genetics research and breeding, Horticulture, Environment, and Biotechnology, 58, 5, (425), (2017).
- Yan-He Li and Han-Ping Wang, Advances of genotyping-by-sequencing in fisheries and aquaculture, Reviews in Fish Biology and Fisheries, 10.1007/s11160-017-9473-2, 27, 3, (535-559), (2017).
- Tomasz Suchan, Anahí Espíndola, Sereina Rutschmann, Brent C. Emerson, Kevin Gori, Christophe Dessimoz, Nils Arrigo, Michał Ronikier and Nadir Alvarez, Assessing the potential of RAD-sequencing to resolve phylogenetic relationships within species radiations: The fly genus Chiastocheta (Diptera: Anthomyiidae) as a case study, Molecular Phylogenetics and Evolution, 114, (189), (2017).
- Girish Kumar and Martin Kocour, Applications of next-generation sequencing in fisheries research: A review, Fisheries Research, 186, (11), (2017).
- M. O. Burford Reiskind, K. Coyle, H. V. Daniels, P. Labadie, M. H. Reiskind, N. B. Roberts, R. B. Roberts, J. Schaff and E. L. Vargo, Development of a universal double‐digest RAD sequencing approach for a group of nonmodel, ecologically and economically important insect and fish taxa, Molecular Ecology Resources, 16, 6, (1303-1314), (2016).
- Molly Schumer, Rongfeng Cui, Daniel L. Powell, Gil G. Rosenthal and Peter Andolfatto, Ancient hybridization and genomic stabilization in a swordtail fish, Molecular Ecology, 25, 11, (2661-2679), (2016).
- CLIVE T. DARWELL, DAVID M. RIVERS and DAVID M. ALTHOFF, RAD‐seq phylogenomics recovers a well‐resolved phylogeny of a rapid radiation of mutualistic and antagonistic yucca moths, Systematic Entomology, 41, 3, (672-682), (2016).
- Emily D. Fountain, Jonathan N. Pauli, Brendan N. Reid, Per J. Palsbøll and M. Zachariah Peery, Finding the right coverage: the impact of coverage and sequence quality on single nucleotide polymorphism genotyping error rates, Molecular Ecology Resources, 16, 4, (966-978), (2016).
- Julia C. Jones, Carmelo Fruciano, Anja Keller, Manfred Schartl and Axel Meyer, Evolution of the elaborate male intromittent organ of Xiphophorus fishes, Ecology and Evolution, 6, 20, (7207-7220), (2016).
- Mercedes Burns and Nobuo Tsurusaki, Male Reproductive Morphology Across Latitudinal Clines and Under Long-Term Female Sex-Ratio Bias, Integrative and Comparative Biology, 56, 4, (715), (2016).
- Zachary W. Culumber and Michael Tobler, Ecological divergence and conservatism: spatiotemporal patterns of niche evolution in a genus of livebearing fishes (Poeciliidae: Xiphophorus), BMC Evolutionary Biology, 10.1186/s12862-016-0593-4, 16, 1, (2016).
- Tomasz Suchan, Camille Pitteloud, Nadezhda S. Gerasimova, Anna Kostikova, Sarah Schmid, Nils Arrigo, Mila Pajkovic, Michał Ronikier, Nadir Alvarez and Ludovic Orlando, Hybridization Capture Using RAD Probes (hyRAD), a New Tool for Performing Genomic Analyses on Collection Specimens, PLOS ONE, 11, 3, (e0151651), (2016).
- Natalia Díaz-Arce, Haritz Arrizabalaga, Hilario Murua, Xabier Irigoien and Naiara Rodríguez-Ezpeleta, RAD-seq derived genome-wide nuclear markers resolve the phylogeny of tunas, Molecular Phylogenetics and Evolution, 102, (202), (2016).
- Tetsumi Takahashi and Teiji Sota, A robust phylogeny among major lineages of the East African cichlids, Molecular Phylogenetics and Evolution, 100, (234), (2016).
- Jeffrey M. DaCosta and Michael D. Sorenson, ddRAD-seq phylogenetics based on nucleotide, indel, and presence–absence polymorphisms: Analyses of two avian genera with contrasting histories, Molecular Phylogenetics and Evolution, 94, (122), (2016).
- Simon Uribe-Convers, Matthew L. Settles, David C. Tank and Berthold Heinze, A Phylogenomic Approach Based on PCR Target Enrichment and High Throughput Sequencing: Resolving the Diversity within the South American Species of Bartsia L. (Orobanchaceae), PLOS ONE, 11, 2, (e0148203), (2016).
- Amber M. Makowicz, Jessie C. Tanner, Eric Dumas, Cameron D. Siler and Ingo Schlupp, Pre-existing biases for swords in mollies (Poecilia), Behavioral Ecology, 27, 1, (175), (2016).
- Carolyn A. Wessinger, Craig C. Freeman, Mark E. Mort, Mark D. Rausher and Lena C. Hileman, Multiplexed shotgun genotyping resolves species relationships within the North American genus Penstemon, American Journal of Botany, 103, 5, (912-922), (2016).
- Martin Stervander, Juan Carlos Illera, Laura Kvist, Pedro Barbosa, Naomi P. Keehnen, Peter Pruisscher, Staffan Bensch and Bengt Hansson, Disentangling the complex evolutionary history of the Western Palearctic blue tits (Cyanistes spp.) – phylogenomic analyses suggest radiation by multiple colonization events and subsequent isolation, Molecular Ecology, 24, 10, (2477-2494), (2015).
- Emily R. Ebel, Jeffrey M. DaCosta, Michael D. Sorenson, Ryan I. Hill, Adriana D. Briscoe, Keith R. Willmott and Sean P. Mullen, Rapid diversification associated with ecological specialization in Neotropical Adelpha butterflies, Molecular Ecology, 24, 10, (2392-2405), (2015).
- Santiago Herrera, Hiromi Watanabe and Timothy M. Shank, Evolutionary and biogeographical patterns of barnacles from deep‐sea hydrothermal vents, Molecular Ecology, 24, 3, (673-689), (2015).
- A. Mastretta‐Yanes, N. Arrigo, N. Alvarez, T. H. Jorgensen, D. Piñero and B. C. Emerson, Restriction site‐associated DNA sequencing, genotyping error estimation and de novo assembly optimization for population genetic inference, Molecular Ecology Resources, 15, 1, (28-41), (2014).
- Jan‐Niklas Macher, Andrey Rozenberg, Steffen U. Pauls, Ralph Tollrian, Rüdiger Wagner and Florian Leese, Assessing the phylogeographic history of the montane caddisfly hremma gallicum using mitochondrial and restriction‐site‐associated DNA (RAD) markers, Ecology and Evolution, 5, 3, (648-662), (2015).
- Ji Hyoun Kang, Tereza Manousaki, Paolo Franchini, Susanne Kneitz, Manfred Schartl and Axel Meyer, Transcriptomics of two evolutionary novelties: how to make a sperm‐transfer organ out of an anal fin and a sexually selected “sword” out of a caudal fin, Ecology and Evolution, 5, 4, (848-864), (2015).
- Nicholas A. Mason and Scott A. Taylor, Differentially expressed genes match bill morphology and plumage despite largely undifferentiated genomes in a Holarctic songbird, Molecular Ecology, 24, 12, (3009-3025), (2015).
- Ingo Braasch, Samuel M. Peterson, Thomas Desvignes, Braedan M. McCluskey, Peter Batzel and John H. Postlethwait, A new model army: Emerging fish models to study the genomics of vertebrate Evo‐Devo, Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 324, 4, (316-341), (2014).
- Tetsumi Takahashi and Edmundo Moreno, A RAD-based phylogenetics for Orestias fishes from Lake Titicaca, Molecular Phylogenetics and Evolution, 93, (307), (2015).
- Braedan M. McCluskey and John H. Postlethwait, Phylogeny of Zebrafish, a “Model Species,” within Danio, a “Model Genus”, Molecular Biology and Evolution, 32, 3, (635), (2015).
- E Pante, J Abdelkrim, A Viricel, D Gey, S C France, M C Boisselier and S Samadi, Use of RAD sequencing for delimiting species, Heredity, 114, 5, (450), (2015).
- Serap Gonen, Stephen C Bishop and Ross D Houston, Exploring the utility of cross-laboratory RAD-sequencing datasets for phylogenetic analysis, BMC Research Notes, 8, 1, (2015).
- Arista Fourie, Michael J. Wingfield, Brenda D. Wingfield and Irene Barnes, Molecular markers delimit cryptic species in Ceratocystis sensu stricto, Mycological Progress, 10.1007/s11557-014-1020-0, 14, 1, (2014).
- Verena A. Kottler, Axel Künstner, Iris Koch, Matthias Flötenmeyer, Tobias Langenecker, Margarete Hoffmann, Eshita Sharma, Detlef Weigel and Christine Dreyer, Adenylate cyclase 5 is required for melanophore and male pattern development in the guppy (Poecilia reticulata), Pigment Cell & Melanoma Research, 28, 5, (545-558), (2015).
- Jeffrey W. Streicher, Thomas J. Devitt, Caren S. Goldberg, John H. Malone, Heath Blackmon and Matthew K. Fujita, Diversification and asymmetrical gene flow across time and space: lineage sorting and hybridization in polytypic barking frogs, Molecular Ecology, 23, 13, (3273-3291), (2014).
- Amélia Viricel, Eric Pante, Willy Dabin and Benoit Simon‐Bouhet, Applicability of RAD‐tag genotyping for interfamilial comparisons: empirical data from two cetaceans, Molecular Ecology Resources, 14, 3, (597-605), (2013).
- Christopher H. Martin and Laura C. Feinstein, Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes, Molecular Ecology, 23, 7, (1846-1862), (2014).
- Paolo Franchini, Carmelo Fruciano, Maria L. Spreitzer, Julia C. Jones, Kathryn R. Elmer, Frederico Henning and Axel Meyer, Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes, Molecular Ecology, 23, 7, (1828-1845), (2013).
- Loren Rieseberg, Tim Vines, Jennifer Gow and Nolan Kane, Editorial 2014, Molecular Ecology, 23, 1, (1-15), (2013).
- Zachary W. Culumber, Pigmentation inXiphophorus: An Emerging System in Ecological and Evolutionary Genetics, Zebrafish, 11, 1, (57), (2014).
- Frederico Henning and Axel Meyer, The Evolutionary Genomics of Cichlid Fishes: Explosive Speciation and Adaptation in the Postgenomic Era, Annual Review of Genomics and Human Genetics, 10.1146/annurev-genom-090413-025412, 15, 1, (417-441), (2014).
- Deren A. R. Eaton, PyRAD: assembly of de novo RADseq loci for phylogenetic analyses, Bioinformatics, 30, 13, (1844), (2014).
- Astrid Cruaud, Mathieu Gautier, Maxime Galan, Julien Foucaud, Laure Sauné, Gwenaëlle Genson, Emeric Dubois, Sabine Nidelet, Thierry Deuve and Jean-Yves Rasplus, Empirical Assessment of RAD Sequencing for Interspecific Phylogeny, Molecular Biology and Evolution, 31, 5, (1272), (2014).
- Tetsumi Takahashi, Nobuaki Nagata and Teiji Sota, Application of RAD-based phylogenetics to complex relationships among variously related taxa in a species flock, Molecular Phylogenetics and Evolution, 80, (137), (2014).
- Nils Offen, Ji Hyoun Kang, Axel Meyer, Gerrit Begemann and Hector Escriva, Retinoic Acid Is Involved in the Metamorphosis of the Anal Fin into an Intromittent Organ, the Gonopodium, in the Green Swordtail (Xiphophorus hellerii), PLoS ONE, 8, 10, (e77580), (2013).
- Shawn R. Narum, C. Alex Buerkle, John W. Davey, Michael R. Miller and Paul A. Hohenlohe, Genotyping‐by‐sequencing in ecological and conservation genomics, Molecular Ecology, 22, 11, (2841-2847), (2013).
- Zachary Baker, Molly Schumer, Yuki Haba, Lisa Bashkirova, Chris Holland, Gil G Rosenthal and Molly Przeworski, Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates, eLife, 10.7554/eLife.24133, 6, (2017).




