Genetic diversity of a widespread annual killifish from coastal Tanzania
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31906845
PubMed Central
PMC6943906
DOI
10.1186/s12862-019-1549-2
PII: 10.1186/s12862-019-1549-2
Knihovny.cz E-zdroje
- Klíčová slova
- Dispersal, Eastern Africa, Historical demography, River morphology, Temporary pool, mtDNA,
- MeSH
- Cyprinodontidae genetika MeSH
- ekosystém * MeSH
- fylogeneze MeSH
- fylogeografie MeSH
- genetická variace * MeSH
- genetický drift MeSH
- mikrosatelitní repetice MeSH
- mitochondriální DNA genetika MeSH
- populační genetika MeSH
- řeky MeSH
- respirační komplex IV genetika MeSH
- sladká voda MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Tanzanie MeSH
- Názvy látek
- mitochondriální DNA MeSH
- respirační komplex IV MeSH
BACKGROUND: African annual killifishes (Nothobranchius spp.) are adapted to seasonally desiccating habitats (ephemeral pools), surviving dry periods as dormant eggs. Given their peculiar life history, geographic aspects of their diversity uniquely combine patterns typical for freshwater taxa (river basin structure and elevation gradient) and terrestrial animals (rivers acting as major dispersal barriers). However, our current knowledge on fine-scale inter-specific and intra-specific genetic diversity of African annual fish is limited to a single, particularly dry region of their distribution (subtropical Mozambique). Using a widespread annual killifish from coastal Tanzania and Kenya, we tested whether the same pattern of genetic divergence pertains to a wet equatorial region in the centre of Nothobranchius distribution. RESULTS: In populations of Nothobranchius melanospilus species group across its range, we genotyped a part of mitochondrial cytochrome oxidase subunit 1 (COI) gene (83 individuals from 22 populations) and 10 nuclear microsatellite markers (251 individuals from 16 populations). We found five lineages with a clear phylogeographic structure but frequent secondary contact. Mitochondrial lineages were largely congruent with main population genetic clusters identified on microsatellite markers. In the upper Wami basin, populations are isolated as a putative Nothobranchius prognathus, but include also a population from a periphery of the middle Ruvu basin. Other four lineages (including putative Nothobranchius kwalensis) coexisted in secondary contact zones, but possessed clear spatial pattern. Main river channels did not form apparent barriers to dispersal. The most widespread lineage had strong signal of recent population expansion. CONCLUSIONS: We conclude that dispersal of a Nothobranchius species from a wet part of the genus distribution (tropical lowland) is not constrained by main river channels and closely related lineages frequently coexist in secondary contact zones. We also demonstrate contemporary connection between the Ruvu and Rufiji river basins. Our data do not provide genetic support for existence of recently described cryptic species from N. melanospilus complex, but cannot resolve this issue.
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Fields PD, Reisser C, Dukić M, Haag CR, Ebert D. Genes mirror geography in Daphnia magna. Mol Ecol. 2015;24:4521–4536. doi: 10.1111/mec.13324. PubMed DOI
Copilaş-Ciocianu D, Zimţa AA, Grabowski M, Petrusek A. Survival in northern microrefugia in an endemic Carpathian gammarid (Crustacea: Amphipoda) Zool Scr. 2018;47:357–372. doi: 10.1111/zsc.12285. DOI
Williams DD. The biology of temporary waters. Oxford: Oxford University Press; 2006.
Berois N, García G, de Sá R. Annual fishes: life history strategy, diversity, and evolution. Boca Raton: CRC Press; 2015.
Watters BR. The ecology and distribution of Nothobranchius fishes. J Am Killifish Assoc. 2009;42:37–76.
Podrabsky JE, Riggs CL, Romney AL, Woll SC, Wagner JT, Culpepper KM, Cleaver TG. Embryonic development of the annual killifish Austrofundulus limnaeus: an emerging model for ecological and evolutionary developmental biology research and instruction. Dev Dyn. 2017;246:779–801. doi: 10.1002/dvdy.24513. PubMed DOI
Reichard M, Polačik M. Nothobranchius furzeri, an 'instant' fish from an ephemeral habitat. eLife. 2019;8:e41548. doi: 10.7554/eLife.41548. PubMed DOI PMC
Furness AI, Reznick DN, Springer MS, Meredith RW. Convergent evolution of alternative developmental trajectories associated with diapause in African and south American killifish. Proc Royal Soc London B. 2015;282:20142189. doi: 10.1098/rspb.2014.2189. PubMed DOI PMC
Furness AI. The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause. Biol Rev. 2016;91:796–812. doi: 10.1111/brv.12194. PubMed DOI
Dorn A, Musilová Z, Platzer M, Reichwald K, Cellerino A. The strange case of east African annual fish: aridification correlates with diversification for a savannah aquatic group? BMC Evol Biol. 2014;14:210. doi: 10.1186/s12862-014-0210-3. PubMed DOI PMC
Nagy B, Cotterill FP, Bellstedt DU. Nothobranchius sainthousei, a new species of annual killifish from the Luapula River drainage in northern Zambia (Teleostei: Cyprinodontiformes) Ichthyol Explor Freshw. 2016;27:233–254.
Nagy B, Watters BR, van der Merwe PDW, Cotterill FPD, Bellstedt DU. Nothobranchius cooperi (Teleostei: Cyprinodontiformes): a new species of annual killifish from the Luapula River drainage, northern Zambia. Afr J Aquat Sci. 2017;42:201–218. doi: 10.2989/16085914.2017.1372270. DOI
Dorn A, Ng’oma E, Janko K, Reichwald K, Polačik M, Platzer M, Cellerino A, Reichard M. Phylogeny, genetic variability and colour polymorphism of an emerging animal model: the short-lived annual Nothobranchius fishes from southern Mozambique. Mol Phylogenet Evol. 2011;61:739–749. doi: 10.1016/j.ympev.2011.06.010. PubMed DOI
Bartáková V, Reichard M, Janko K, Polačik M, Blažek R, Reichwald K, Cellerino A, Bryja J. Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique. BMC Evol Biol. 2013;13:196. doi: 10.1186/1471-2148-13-196. PubMed DOI PMC
Bartáková V, Reichard M, Blažek R, Polačik M, Bryja J. Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna. J Biogeogr. 2015;42:1832–1844. doi: 10.1111/jbi.12567. DOI
Wildekamp RH. A world of Killies: atlas of the oviparous Cyprinodontiform fishes of the world. Elyria: American Killifish Association; 2004.
Costa WJEM. Two new species of seasonal killifishes of the Nothobranchius melanospilus species complex from the East Africa biodiversity hotspot (Cyprinodontiformes: Aplocheilidae) Vert Zool. 2019;69:73–82.
Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403:853. doi: 10.1038/35002501. PubMed DOI
Azeria ET, Sanmartín I, Ås S, Carlson A, Burgess N. Biogeographic patterns of the east African coastal forest vertebrate fauna. Biodivers Conserv. 2007;16:883–912. doi: 10.1007/s10531-006-9022-0. DOI
Wildekamp RH, Shidlovskiy KM, Watters BR. Systematics of the Nothobranchius melanospilus species group (Cyprinodontiformes: Nothobranchiidae) with description of two new species from Tanzania and Mozambique. Ichthyol Explor Freshw. 2009;20:237.
Costa WJEM. Taxonomic revision of the seasonal killifish genus Nothobranchius from Zanzibar, East Africa (Cyprinodontoidei: Aplocheilidae) J Nat Hist. 2017;51:1609–1624. doi: 10.1080/00222933.2017.1330976. DOI
Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol. 2016;34:772–773. PubMed
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC
Miller MA, Pfeiffer W, Schwart T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans: IEEE; 2010. p. 1–8.
Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–1452. doi: 10.1093/bioinformatics/btp187. PubMed DOI
Fahey AL, Ricklefs RE, DeWoody JA. DNAbased approaches for evaluating historical demography in terrestrial vertebrates. Biol J Linn Soc. 2014;112:367–386. doi: 10.1111/bij.12259. DOI
Schneider S, Excoffier L. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics. 1999;152:1079–1089. PubMed PMC
Rogers A. Genetic evidence for a Pleistocene population explosion. Evolution. 1995;49:608–615. doi: 10.1111/j.1558-5646.1995.tb02297.x. PubMed DOI
Excoffier L, Laval G, Schneider S. ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform. 2005;1:47–50. doi: 10.1177/117693430500100003. PubMed DOI PMC
Chapuis M-P, Estoup A. Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol. 2007;24:621–631. doi: 10.1093/molbev/msl191. PubMed DOI
Raymond M, Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered. 1995;86:248–249. doi: 10.1093/oxfordjournals.jhered.a111573. DOI
Rousset F. genepop’007: a complete re-implementation of the genepop software for windows and Linux. Mol Ecol Resour. 2008;8:103–106. doi: 10.1111/j.1471-8286.2007.01931.x. PubMed DOI
Storey JD. A direct approach to false discovery rates. J R Stat Soc Series B. 2002;64:479–498. doi: 10.1111/1467-9868.00346. DOI
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. Laboratoire Génome, Populations, Interactions, CNRS UMR. 1996. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations; p. 5000.
Goudet J. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available at https://kimura.univ-montp2.fr/genetix. Accessed 2 Dec 2019.
Hubisz MJ, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Mol Ecol Res. 2009;9:1322–1332. doi: 10.1111/j.1755-0998.2009.02591.x. PubMed DOI PMC
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 2015;15:1179–1191. doi: 10.1111/1755-0998.12387. 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;14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x. PubMed DOI
Wildekamp RW. Back to the theme Nothobranchius guentheri and Nothobranchius melanospilus, with additional notes to the N. melanospilus complex sensu Costa 2019. JAKA. 2019;52:43–52.
Vrtílek M, Reichard M. Patterns of morphological variation among populations of the widespread annual killifish Nothobranchius orthonotus are independent of genetic divergence and biogeography. J Zool Syst Evol Res. 2016;54:289–298. doi: 10.1111/jzs.12134. DOI
Reichard M. The evolutionary ecology of African annual fishes. In: Berois N, García G, de Sá R, editors. Annual Fishes: Life History Strategy, Diversity, and Evolution: CRC Press; 2015. p. 133–58.
Vrtílek M, Žák J, Polačik M, Blažek R, Reichard M. Longitudinal demographic study of wild populations of African annual killifish. Sci Rep. 2018;8:4774. doi: 10.1038/s41598-018-22878-6. PubMed DOI PMC
Vrtílek M, Žák J, Pšenička M, Reichard M. Extremely rapid maturation of a wild African annual fish. Curr Biol. 2018;28:R822–R824. doi: 10.1016/j.cub.2018.06.031. PubMed DOI
Lambert JW, Reichard M, Pincheira-Donoso D. Live fast, diversify non-adaptively: evolutionary diversification of exceptionally short-lived annual killifishes. BMC Evol Biol. 2019;19:10. doi: 10.1186/s12862-019-1344-0. PubMed DOI PMC
de León JLP, León G, Rodríguez R, Metcalfe CJ, Hernández D, Casane D, García-Machado E. Phylogeography of Cuban Rivulus: evidence for allopatric speciation and secondary dispersal across a marine barrier. Mol Phylogenet Evol. 2014;79:404–414. doi: 10.1016/j.ympev.2014.07.007. PubMed DOI
Duvernell DD, Meier SL, Schaefer JF, Kreiser BR. Contrasting phylogeographic histories between broadly sympatric topminnows in the Fundulus notatus species complex. Mol Phylogenet Evol. 2013;69:653–663. doi: 10.1016/j.ympev.2013.07.013. PubMed DOI
Adams SM, Lindmeier JB, Duvernell DD. Microsatellite analysis of the phylogeography, Pleistocene history and secondary contact hypotheses for the killifish, Fundulus heteroclitus. Mol Ecol. 2006;15:1109–1123. doi: 10.1111/j.1365-294X.2006.02859.x. PubMed DOI
García G, Gutiérrez V, Vergara J, Calvino P, Duarte A, Loureiro M. Patterns of population differentiation in annual killifishes from the Paraná–Uruguay–La Plata Basin: the role of vicariance and dispersal. J Biogeogr. 2012;39:1707–1719. doi: 10.1111/j.1365-2699.2012.02722.x. DOI
Dutton A, Lambeck K. Ice volume and sea level during the last interglacial. Science. 2012;337:216–219. doi: 10.1126/science.1205749. PubMed DOI
Cohen AS, Stone JR, Beuning KRM, Park LE, Reinthal PZ, Dettman D, Scholz CA, Johnson TC, King JW, Talbot MR, Brown ET, Ivory SJ. Ecological consequences of early late Pleistocene megadroughts in tropical Africa. Proc Natl Acad Sci U S A. 2007;104:16422–16427. doi: 10.1073/pnas.0703873104. PubMed DOI PMC
Lorenzen ED, Heller R, Siegismund HR. Comparative phylogeography of African savannah ungulates. Mol Ecol. 2012;21:3656–3670. doi: 10.1111/j.1365-294X.2012.05650.x. PubMed DOI
Le Gall B, Gernigon L, Rolet J, Ebinger C, Gloaguen R, Nilsen O, Dypvig H, Deffontaines B, Mruma A. Neogene-Holocene rift propagation in Central Tanzania: Morphostructural and aeromagnetic evidence from the Kilombero area. GSA Bull. 2004;116:490–5 10. doi: 10.1130/B25202.1. DOI
Vincens A, Garcin Y, Buchet G. Influence of rainfall seasonality on African lowland vegetation during the Late Quaternary: pollen evidence from Lake Masoko, Tanzania. J Biogeogr. 2007;34:1274–1288. doi: 10.1111/j.1365-2699.2007.01698.x. DOI
Goodier SA, Cotterill FP, 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:e28775. doi: 10.1371/journal.pone.0028775. PubMed DOI PMC
Wu TH, Tsang LM, Chen I-S, Chu KH. Multilocus approach reveals cryptic lineages in the goby Rhinogobius duospilus in Hong Kong streams: role of paleodrainage systems in shaping marked population differentiation in a city. Mol Phyl Evol. 2016;104:112–122. doi: 10.1016/j.ympev.2016.07.014. PubMed DOI
Perea S, Doadrio I. Phylogeography, historical demography and habitat suitability modelling of freshwater fishes inhabiting seasonally fluctuating Mediterranean river systems: a case study using the Iberian cyprinid Squalius valentinus. Mol Ecol. 2015;24:3706–3722. doi: 10.1111/mec.13274. PubMed DOI
Tweddle D, van der Waal BCW, Peel RA. Distribution and migration of the Caprivi killifish Nothobranchius caprivensis Watters, Wildekamp, Shidlovskiy 2015, an assessment of its conservation status and a note of other killifish in the same area. J Am Killifish Assoc. 2014;47:134–151.
Cellerino A, Valenzano DR, Reichard M. From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol Rev. 2016;91:511–533. doi: 10.1111/brv.12183. PubMed DOI
Giddelo CS, Arndt AD, Volckaert FAM. Impact of rifting and hydrography on the genetic structure of Clarias gariepinus in eastern Africa. J Fish Biol. 2002;60:1252–1266. doi: 10.1111/j.1095-8649.2002.tb01718.x. DOI
Kaaya LT. Towards a classification of Tanzanian rivers: a bioassessment and ecological management tool. A case study of the Pangani, Rufiji and Wami–Ruvu river basins. Afr. J Aquat Sci. 2015;40:37–45. doi: 10.2989/16085914.2015.1008970. DOI
Patterns and drivers of Nothobranchius killifish diversity in lowland Tanzania
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