Biogeographical and ecological barriers strongly affect the course of micro-evolutionary processes in free living organisms. Here we assess the impact of a recently emerged barrier on populations of limnic fauna. Genetic diversity and population structure in a host-parasite system (Wenyonia virilis tapeworm, Synodontis schall catfish) are analyzed in the recently divided Turkana and Nile basins. The two basins, were repeatedly connected during the Holocene wet/dry climatic oscillations, following late Pleistocene dessication of the Turkana basin. Mitochondrial DNA sequences for cytochrome oxidase I gene (cox I) and a whole genome scanning method-amplified fragment length polymorphism (AFLP) were employed. A total of 347 cox I sequences (representing 209 haplotypes) and 716 AFLP fragments, as well as 120 cox I sequences (20 haplotypes) and 532 AFLP fragments were obtained from parasites and hosts, respectively. Although results indicate that host and parasite populations share some formative traits (bottlenecks, Nilotic origin), their population histories/patterns differ markedly. Mitochondrial analysis revealed that parasite populations evolve significantly faster and show remarkably higher genetic variability. Analyses of both markers confirmed that the parasites undergo lineage fission, forming new clusters specific for either freshwater or saline parts of Lake Turkana. In congruence with the geological history, these clusters apparently indicate multiple colonisations of Lake Turkana from the Nile. In contrast, the host population pattern indicates fusion of different colonisation waves. Although fish host populations remain connected, saline habitats in Lake Turkana (absent in the Nile), apparently pose a barrier to the gene flow in the parasite, possibly due to its multihost lifecycle, which involves freshwater annelids. Despite partially corroborating mitochondrial results, AFLP data was not sufficiently informative for analyzing populations with recently mixed biogeographic histories.

Faculty of Science University of South Bohemia Branišovská České Budějovice Czech Republic

Institute of Parasitology Biology Centre Czech Academy of Sciences Branišovská České Budějovice Czech Republic

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Hewitt GM. Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond B Biol Sci. 2004;359: 183–195; discussion 195. 10.1098/rstb.2003.1388 PubMed DOI PMC

Behrensmeyer AK, Todd NE, Potts R, Mcbrinn GE. Late Pliocene Faunal Turnover in the Turkana Basin, Kenya and Ethiopia. Science. 1997;278: 1589–1594. PubMed

McKee JK. Faunal Turnover Rates and Mammalian Biodiversity of the Late Pliocene and Pléistocene of Eastern Africa. Paleobiology. 2001;27: 500–511.

Weber W, White L, Vedder A, Naughton-Treves L. The African rain forest: climate and vegetation In: Weber W, Veder A, Simons Morland H, White LJT, Hart TB, editors. African Rain Forest Ecology and Conservation An Interdisciplinary Perspective. Yale University Press; 2001. pp. 3–29.

Hewitt GM. Some genetic consequences of ice ages, and their role, in divergence and speciation. Biol J Linn Soc. 1996;58: 247–276.

Matthee CA, Tilbury CR, Townsend T. A phylogenetic review of the African leaf chameleons: genus Rhampholeon (Chamaeleonidae): the role of vicariance and climate change in speciation. Proc Biol Sci / R Soc. 2004;271: 1967–1975. PubMed PMC

Mariaux J, Lutzmann N, Stipala J. The two-horned chamaeleons of East Africa. Zool J Linn Soc. 2008;152: 367–391.

Day JJ, Peart CR, Brown KJ, Friel JP, Bills R, Moritz T. Continental diversification of an African catfish radiation (Mochokidae: Synodontis). Syst Biol. 2013;62: 351–365. 10.1093/sysbio/syt001 PubMed DOI

Otero O, Gayet M. Palaeoichthyofaunas from the Lower Oligocene and Miocene of the Arabian Plate: Palaeoecological and palaeobiogeographical implications. Palaeogeogr Palaeoclimatol Palaeoecol. 2001;165: 141–169.

Stewart KM. The freshwater fish of Neogene Africa (Miocene-Pleistocene): Systematics and biogeography. Fish Fish. 2001;2: 177–230.

Elmer KR, Reggio C, Wirth T, Verheyen E, Salzburger W, Meyer A. Pleistocene desiccation in East Africa bottlenecked but did not extirpate the adaptive radiation of Lake Victoria haplochromine cichlid fishes. Proc Natl Acad Sci U S A. 2009;106: 13404–13409. 10.1073/pnas.0902299106 PubMed DOI PMC

Kautt AF, Elmer KR, Meyer A. Genomic signatures of divergent selection and speciation patterns in a “natural experiment”, the young parallel radiations of Nicaraguan crater lake cichlid fishes. Mol Ecol. 2012;21: 4770–86. 10.1111/j.1365-294X.2012.05738.x PubMed DOI

Lundberg JG, Marshall LG, Guerrero J, Horton B, Malabarba MCSL, Wesselingh F. The stage for neotropical fish diversification a history of tropical south american rivers. Phylogeny and Classification of Neotropical Fishes. 1998. p. 603.

Montoya-Burgos JI. Historical biogeography of the catfish genus Hypostomus (Siluriformes: Loricariidae), with implications on the diversification of Neotropical ichthyofauna. Mol Ecol. 2003;12: 1855–1867. PubMed

Goodier SAM, Cotterill FPD, O’Ryan C, Skelton PH, de Wit MJ. Cryptic Diversity of African Tigerfish (Genus Hydrocynus) Reveals Palaeogeographic Signatures of Linked Neogene Geotectonic Events. PLoS One. 2011;6. PubMed PMC

Pinton A, Agnèse J-F, Paugy D, Otero O. A large-scale phylogeny of Synodontis (Mochokidae, Siluriformes) reveals the influence of geological events on continental diversity during the Cenozoic. Mol Phylogenet Evol. 2013;66: 1027–40. 10.1016/j.ympev.2012.12.009 PubMed DOI

Wagner CE, Harmon LJ, Seehausen O. Cichlid species-area relationships are shaped by adaptive radiations that scale with area. Ecol Lett. 2014;17: 583–92. 10.1111/ele.12260 PubMed DOI

Johnson TC, Malala JO. The Nile: Origin, Environments, Lymnology and Human Use Lake Turkana and its link to the Nile. Springer Science+Business Media BV; 2009. pp. 287–302.

Bloszies C, Forman SL, Wright DK. Water level history for Lake Turkana, Kenya in the past 15,000years and a variable transition from the African Humid Period to Holocene aridity. Glob Planet Change. Elsevier B.V.; 2015;132: 64–76.

Friesen VL, Smith AL, Gómez-Díaz E, Bolton M, Furness RW, González-Solís J, et al. Sympatric speciation by allochrony in a seabird. Proc Natl Acad Sci U S A. 2007;104: 18589–18594. 10.1073/pnas.0700446104 PubMed DOI PMC

Rolshausen G, Segelbacher G, Hobson KA, Schaefer HM. Contemporary Evolution of Reproductive Isolation and Phenotypic Divergence in Sympatry along a Migratory Divide. Curr Biol. Elsevier Ltd; 2009;19: 2097–2101. PubMed

Berg PR, Jentoft S, Star B, Ring KH, Knutsen H, Lien S, et al. Adaptation to low salinity promotes genomic divergence in Atlantic Cod (Gadus morhua L.). Genome Biol Evol. 2015;7: 1644–1663. 10.1093/gbe/evv093 PubMed DOI PMC

Dumont HJ. A Description of the Nile Basin, and a Synopsis of Its History, Ecology, Biogeography, Hydrology, and Natural Resources Nile. 2009; 1–21.

Harvey CPD, Grove AT. A Prehistoric Source of the Nile. Geogr J. 1982;148: 327–336. Available: http://www.jstor.org/stable/633150

Nyamweru C. New Evidence for the Former Extent of the Nile Drainage System. Geogr J. Blackwell Publishing on behalf of The Royal Geographical Society (with the Institute of British Geographers); 1989;155: 179–188. Available: http://www.jstor.org/stable/635059

Ricketts RD, Anderson RF. A Direct Comparison Between the Historical Record of Lake Level and the δ18O Signal in Carbonate Sediments from Lake Turkana, Kenya. Limnol Oceanogr. American Society of Limnology and Oceanography; 1998;43: 811–822. Available: http://www.jstor.org/stable/2839176

Hopson A. Lake Turkana; A Report on the Finding of the Lake Turkana Project 1972–1975, Vols. 1–6. Overseas Development Administration, London; 1982.

Camberlin P. Nile Basin Climates The Nile: Origin, Environments, Limnology and Human Use. 2009. pp. 307–333.

Barrows TT, Williams MAJ, Mills SC, Duller GAT, Fifield LK, Haberlah D, et al. A White Nile megalake during the last interglacial period. Geology. 2014;42: 163–166.

Froese R, Pauly D. FishBase [Internet]. Version 2015.8. 2014. p. www.fishbase.org. www.fishbase.org

Schaeffner BC, Jirků M, Mahmoud ZN, Scholz T. Revision of Wenyonia Woodland, 1923 (Cestoda: Caryophyllidea) from catfishes (Siluriformes) in Africa. Syst Parasitol. 2011;79: 83–107. 10.1007/s11230-011-9290-2 PubMed DOI

Mackiewicz JS. Caryophyllidea (Cestoidea): a review. Exp Parasitol. 1972;31: 417–512. PubMed

Scholz T, Brabec J, Kráĺová-Hromadová I, Oros M, Bazsalovicsová E, Ermolenko A, et al. Revision of Khawia spp. (Cestoda: Caryophyllidea), parasites of cyprinid fish, including a key to their identification and molecular phylogeny. Folia Parasitol (Praha). 2011;58: 197–223. PubMed

Scholz T, Hanzelová V. Tapeworms of the genus Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), parasites of fishes in Europe. Praha Acad Stud AV ČR; 1998; 119 pp.

Sambrook J, Russell DW. Molecular Cloning—Sambrook & Russel. Human Mutation. 2001.

Werle E, Schneider C, Renner M, Völker M, Fiehn W. Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Res. 1994;22: 4354–4355. PubMed PMC

Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN. Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes. 2007;7: 544–548.

Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995;23: 4407–14. Available: http://www.ncbi.nlm.nih.gov/pubmed/10206688 PubMed PMC

Tandon R, Lyons ET, Tolliver SC, Kaplan RM. Effect of moxidectin selection on the genetic variation within Cylicocyclus nassatus based on amplified fragment length polymorphism (AFLP). Int J Parasitol. 2005;35: 813–9. 10.1016/j.ijpara.2005.02.004 PubMed DOI

de Gruijter JM, Polderman AM, Dijkshoorn L, Roberts H, Ziem J, Kunwar CB, et al. AFLP fingerprinting for the analysis of genetic diversity within Necator americanus. Mol Cell Probes. 2006;20: 317–21. 10.1016/j.mcp.2006.03.004 PubMed DOI

Nejsum P, Grøndahl C, Murrell KD. Molecular evidence for the infection of zoo chimpanzees by pig Ascaris. Vet Parasitol. 2006;139: 203–10. 10.1016/j.vetpar.2006.02.025 PubMed DOI

Patra KP, Ramu T, Hoti SL, Pragasam GS, Das PK. Identification of a molecular marker for genotyping human lymphatic filarial nematode parasite Wuchereria bancrofti. Exp Parasitol. 2007;116: 59–65. 10.1016/j.exppara.2006.11.011 PubMed DOI

Mattersdorfer K, Koblmüller S, Sefc KM. AFLP genome scans suggest divergent selection on colour patterning in allopatric colour morphs of a cichlid fish. Mol Ecol. 2012;21: 3531–44. 10.1111/j.1365-294X.2012.05634.x PubMed DOI

Xu D, Lou B, Xu H, Li S, Geng Z. Isolation and Characterization of Male-Specific DNA Markers in the Rock Bream Oplegnathus fasciatus. Mar Biotechnol (NY). 2013;15: 221–9. PubMed

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28: 1647–1649. 10.1093/bioinformatics/bts199 PubMed DOI PMC

Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30: 3059–3066. PubMed PMC

Posada D. jModelTest: Phylogenetic model averaging. Mol Biol Evol. 2008;25: 1253–1256. 10.1093/molbev/msn083 PubMed DOI

Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology. Science. 2001;294: 2310–2314. 10.1126/science.1065889 PubMed DOI

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19: 1572–1574. PubMed

Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL. AWTY (are we there yet?): A system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics. 2008;24: 581–583. 10.1093/bioinformatics/btm388 PubMed DOI

Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52: 696–704. PubMed

Hasegawa M, Kishino H, Yano TA. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22: 160–174. PubMed

Gascuel O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol. 1997;14: 685–695. PubMed

Brandley MC, Schmitz A, Reeder TW. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst Biol. 2005;54: 373–90. 10.1080/10635150590946808 PubMed DOI

Lanfear R, Calcott B, Ho SYW, Guindon S. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol. 2012;29: 1695–1701. 10.1093/molbev/mss020 PubMed DOI

Rambaut A, Drummond AJ. Tracer V1.5. http://beast.bio.ed.ac.uk/Tracer. 2009;

Zwickl DJ. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Philosophy. 2006; 115. (http://www.zo.utexas.edu/faculty/antisense/garli/Garli.html)

Leigh JW, Bryant D. Popart: Full-Feature Software for Haplotype Network Construction. Methods Ecol Evol. 2015;6: 1110–1116.

Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25: 1451–2. 10.1093/bioinformatics/btp187 PubMed DOI

Beerli P. MIGRATE: documentation and program, part of LAMARC. http://evolution.genetics.washington.edu/lamarc.html. 1997;

Kass RE, Raftery AE. Bayes Factors. J Am Stat Assoc. American Statistical Association; 1995;90: 773–795.

Beerli P, Palczewski M. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics. 2010;185: 313–26. 10.1534/genetics.109.112532 PubMed DOI PMC

Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics. 2012;28: 2537–2539. 10.1093/bioinformatics/bts460 PubMed DOI PMC

Antao T, Beaumont MA. Mcheza: a workbench to detect selection using dominant markers. Bioinformatics. 2011;27: 1717–8. 10.1093/bioinformatics/btr253 PubMed DOI

Hubisz MJ, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour. 2009;9: 1322–1332. 10.1111/j.1755-0998.2009.02591.x PubMed DOI PMC

Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14: 2611–20. 10.1111/j.1365-294X.2005.02553.x PubMed DOI

Jakobsson M, Rosenberg NA. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23: 1801–1806. 10.1093/bioinformatics/btm233 PubMed DOI

Rosenberg NA. DISTRUCT: A program for the graphical display of population structure. Mol Ecol Notes. 2004;4: 137–138.

Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7: 214 10.1186/1471-2148-7-214 PubMed DOI PMC

Štefka J, Hoeck PEA, Keller LF, Smith VS. A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites. BMC Evol Biol. 2011;11: 284 10.1186/1471-2148-11-284 PubMed DOI PMC

Johnson KP, Allen JM, Olds BP, Mugisha L, Reed DL, Paige KN, et al. Rates of genomic divergence in humans, chimpanzees and their lice. Proc Biol Sci. 2014;281: 20132174 10.1098/rspb.2013.2174 PubMed DOI PMC

Hafner M, Sudman P, Villablanca F, Spradling T, Demastes J, Nadler S. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science. 1994;265: 1087–1090. PubMed

Kaltz O, Shykoff JA. Local adaptation in host—parasite systems. Heredity (Edinb). 1998;81: 361–370.

Gandon S, Michalakis Y. Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. J Evol Biol. 2002;15: 451–462.

Frank SA. Evolution of host-parasite diversity. Evolution (N Y). JSTOR; 1993;47: 1721–1732. PubMed

Day T, Graham AL, Read AF. Evolution of parasite virulence when host responses cause disease. Proc Biol Sci. 2007;274: 2685–2692. 10.1098/rspb.2007.0809 PubMed DOI PMC

Best A, White A, Boots M. The Implications of Coevolutionary Dynamics to Host-Parasite Interactions. Source Am Nat. 2009;173: 779–791. Available: http://www.jstor.org/stable/10.1086/598494%5Cnhttp://www.jstor.org/page/info/about/policies/terms.jsp%5Cnhttp://www.jstor.org PubMed DOI

Cohuet A, Harris C, Robert V, Fontenille D. Evolutionary forces on Anopheles: what makes a malaria vector? Trends Parasitol. Elsevier Ltd; 2010;26: 130–136. PubMed

Khan SM, Reece SE, Waters AP, Janse CJ, Kaczanowski S. Why are male malaria parasites in such a rush?: Sex-specific evolution and host-parasite interactions. Evol Med public Heal. 2013;2013: 3–13. PubMed PMC

Emerson BC, Faria CMA. Fission and fusion in island taxa—serendipity, or something to be expected? Mol Ecol. 2014;23: 5132–5134. 10.1111/mec.12951 PubMed DOI

Garrick RC, Benavides E, Russello MA, Hyseni C, Edwards DL, Gibbs JP, et al. Lineage fusion in Galápagos giant tortoises. Mol Ecol. 2014;23: 5276–5290. 10.1111/mec.12919 PubMed DOI

Sexton JP, Hangartner SB, Hoffmann AA. Genetic isolation by environment or distance: Which pattern of gene flow is most common? Evolution (N Y). 2014;68: 1–15. PubMed

Orsini L, Vanoverbeke J, Swillen I, Mergeay J, De Meester L. Drivers of population genetic differentiation in the wild: Isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Molecular Ecology. 2013. pp. 5983–5999. 10.1111/mec.12561 PubMed DOI

Spurgin LG, Illera JC, Jorgensen TH, Dawson DA, Richardson DS. Genetic and phenotypic divergence in an island bird: Isolation by distance, by colonization or by adaptation? Mol Ecol. 2014;23: 1028–1039. 10.1111/mec.12672 PubMed DOI

Hughes J, Kennedy M, Johnson KP, Palma RL, Page RDM. Multiple cophylogenetic analyses reveal frequent cospeciation between pelecaniform birds and Pectinopygus lice. Syst Biol. 2007;56: 232–251. 10.1080/10635150701311370 PubMed DOI

Koop JAH, DeMatteo KE, Parker PG, Whiteman NK. Birds are islands for parasites. Biol Lett. 2014;10: 6–10. PubMed PMC

Otsen M, Hoekstra R, Plas ME, Buntjer JB, Lenstra JA, Roos MH. Amplied fragment length polymorphism analysis of genetic diversity of Haemonchus contortus during selection for drug resistance. Int J Parasitol. 2001;31: 1138–1143. PubMed

Van Der Veer M, De Vries E. Genetic intrapopulation variation, revealed by amplified fragment length polymorphism, within a population of the trichostrongylid nematode Cooperia oncophora. Exp Parasitol. 2003;104: 70–73. PubMed

Roos MH, Otsen M, Hoekstra R, Veenstra JG, Lenstra JA. Genetic analysis of inbreeding of two strains of the parasitic nematode Haemonchus contortus. Int J Parasitol. 2004;34: 109–115. PubMed

Simo G, Cuny G, Demonchy R, Herder S. Trypanosoma brucei gambiense: study of population genetic structure of Central African stocks using amplified fragment length polymorphism (AFLP). Exp Parasitol. 2008;118: 172–80. 10.1016/j.exppara.2007.07.010 PubMed DOI

Dasmahapatra KK, Elias M, Hill RI, Hoffman JI, Mallet J. Mitochondrial DNA barcoding detects some species that are real, and some that are not. Mol Ecol Resour. 2010;10: 264–273. 10.1111/j.1755-0998.2009.02763.x PubMed DOI

Folkertsma RT, Rouppe van der Voort JN, de Groot KE, van Zandvoort PM, Schots A, Gommers FJ, et al. Gene pool similarities of potato cyst nematode populations assessed by AFLP analysis. Mol Plant Microbe Interact. 1996;9: 47–54. PubMed

Gaudet M, Jorge V, Paolucci I, Beritognolo I, Mugnozza GS, Sabatti M. Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait. Tree Genet Genomes. 2007;4: 25–36.

Frascaroli E, Schrag TA, Melchinger AE. Genetic diversity analysis of elite European maize (Zea mays L.) inbred lines using AFLP, SSR, and SNP markers reveals ascertainment bias for a subset of SNPs. Theor Appl Genet. 2013;126: 133–41. 10.1007/s00122-012-1968-6 PubMed DOI

Martinelli A, Hunt P, Cheesman SJ, Carter R. Amplified fragment length polymorphism measures proportions of malaria parasites carrying specific alleles in complex genetic mixtures. Mol Biochem Parasitol. 2004;136: 117–122. PubMed

From taxonomic deflation to newly detected cryptic species: Hidden diversity in a widespread African squeaker catfish