Population structure, inbreeding and stripe pattern abnormalities in plains zebras.
Equus quagga
inbreeding
population genomics
stripe pattern
zebra
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
30
06
2020
revised:
23
10
2020
accepted:
30
10
2020
pubmed:
12
11
2020
medline:
22
6
2021
entrez:
11
11
2020
Statut:
ppublish
Résumé
One of the most iconic wild equids, the plains zebra occupies a broad region of sub-Saharan Africa and exhibits a wide range of phenotypic diversity in stripe patterns that have been used to classify multiple subspecies. After decades of relative stability, albeit with a loss of at least one recognized subspecies, the total population of plains zebras has undergone an approximate 25% decline since 2002. Individuals with abnormal stripe patterns have been recognized in recent years but the extent to which their appearance is related to demography and/or genetics is unclear. Investigating population genetic health and genetic structure are essential for developing effective strategies for plains zebra conservation. We collected DNA from 140 plains zebra, including seven with abnormal stripe patterns, from nine locations across the range of plains zebra, and analyzed data from restriction site-associated and whole genome sequencing (RAD-seq, WGS) libraries to better understand the relationships between population structure, genetic diversity, inbreeding, and abnormal phenotypes. We found that genetic structure did not coincide with described subspecific variation, but did distinguish geographic regions in which anthropogenic habitat fragmentation is associated with reduced gene flow and increased evidence of inbreeding, especially in certain parts of East Africa. Further, zebras with abnormal striping exhibited increased levels of inbreeding relative to normally striped individuals from the same populations. Our results point to a genetic cause of stripe pattern abnormalities, and dramatic evidence of the consequences of habitat fragmentation.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
379-390Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Alexander, D. H., Novembre, J., & Lange, K. (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19(9), 1655-1664. https://doi.org/10.1101/gr.094052.109
Anderson, E. C., & Dunham, K. K. (2008). The influence of family groups on inferences made with the program Structure. Molecular Ecology Resources, 8(6), 1219-1229. https://doi.org/10.1111/j.1755-0998.2008.02355.x
Avise, J. (1989). A role for molecular genetics in the recognitiion and conservation of endangered species. Trends in Ecology & Evolution, 4, 279-281.
Bartlam-Brooks, H. L. A., Bonyongo, M. C., & Harris, S. (2011). Will reconnecting ecosystems allow long-distance mammal migrations to resume? A case study of a zebra Equus burchelli migration in Botswana. Oryx, 45(02), 210-216. https://doi.org/10.1017/s0030605310000414
Brown, D. M., Brenneman, R. A., Koepfli, K.-P., Pollinger, J. P., Milá, B., Georgiadis, N. J., Louis, E. E., Grether, G. F., Jacobs, D. K., & Wayne, R. K. (2007). Extensive population genetic structure in the giraffe. BMC Biology, 5, 57. https://doi.org/10.1186/1741-7007-5-57
Caputo, M., Rubenstein, D. I., Froneman, P. W., & Bouveroux, T. (2018). Striping patterns may not influence social interactions and mating in zebra: Observations from melanic zebra in South Africa. African Journal of Ecology, 56(2), 428-431. https://doi.org/10.1111/aje.12463
Caro, T., & Stankowich, T. (2015). Concordance on zebra stripes: A comment on Larison et al (2015). Royal Society Open Science, 2(9), 150323. https://doi.org/10.1098/rsos.150323
Ceballos, F. C., Joshi, P. K., Clark, D. W., Ramsay, M., & Wilson, J. F. (2018). Runs of homozygosity: Windows into population history and trait architecture. Nature Reviews Genetics, 19(4), 220-234. https://doi.org/10.1038/nrg.2017.109
Cobb, A., & Cobb, S. (2019). Do zebra stripes influence thermoregulation? Journal of Natural History, 53(13-14), 863-879. https://doi.org/10.1080/00222933.2019.1607600
Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M., & Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution, 15(7), 290-295. https://doi.org/10.1016/S0169-5347(00)01876-0
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., Durbin, R., &1000 Genomes Project Analysis Group. (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156-2158. https://doi.org/10.1093/bioinformatics/btr330
Druce, D. (2020). [Park Ecologist, Exembelo KwaZulu-Natal Wildlife].
Epps, C. W., Castillo, J. A., Schmidt-Küntzel, A., Preez, P. D., Stuart-Hill, G., Jago, M., & Naidoo, R. (2013). Contrasting historical and recent gene flow among African buffalo herds in the Caprivi strip of Namibia. Journal of Heredity, 104(2), 172-181. https://doi.org/10.1093/jhered/ess142
Etter, P. D., Bassham, S., Hohenlohe, P. A., Johnson, E. A., & Cresko, W. A. (2011). SNP discovery and genotyping for evolutionary genetics using RAD sequencing. Methods in Molecular Biology, 772, 157-178. https://doi.org/10.1007/978-1-61779-228-1_9
Fynn, R. W. S., & Bonyongo, M. C. (2011). Functional conservation areas and the future of Africa's wildlife. African Journal of Ecology, 49(2), 175-188. https://doi.org/10.1111/j.1365-2028.2010.01245.x
Garrison, E., & Marth, G. (2012). Haplotype-based variant detection from short-read sequencing. arXiv:1207:3907 [q-bio.GN].
Groves, C. P., & Bell, C. H. (2004). New invesitgations on the taxonomy of the zebras genus Equus, subgenus Hippotigris. Mammalian Biology, 69(3), 182-196.
Hack, M. A., East, R., & Rubenstein, D. I. (2002). Status and action plan for the plains Zebra. In P. D. Moehlman (Ed.), Equids: Zebras, asses and horses. status survey and conservation action plan (pp. 43-60). : IUCN/SSC Equid Specialist Group, IUCN.
Harris, G., Thirgood, S., Hopcraft, J. G. C., Cromsight, J., & Berger, J. (2009). Global decline in aggregated migrations of large terrestrial mammals. Endangered Species Research, 7, 55-76. https://doi.org/10.3354/esr00173
Hayward, M. W., & Kerley, G. I. H. (2009). Fencing for conservation: Restriction of evolutionary potential or a riposte to threatening processes? Biological Conservation, 142(1), 1-13. https://doi.org/10.1016/j.biocon.2008.09.022
Heller, R., Lorenzen, E. D., Okello, J. B., Masembe, C., & Siegismund, H. R. (2008). Mid-Holocene decline in African buffalos inferred from Bayesian coalescent-based analyses of microsatellites and mitochondrial DNA. Molecular Ecology, 17(22), 4845-4858. https://doi.org/10.1111/j.1365-294X.2008.03961.x
Howrigan, D. P., Simonson, M. A., & Keller, M. C. (2011). Detecting autozygosity through runs of homozygosity: A comparison of three autozygosity detection algorithms. BMC Genomics, 12(1), 460. https://doi.org/10.1186/1471-2164-12-460
Broad Institute. (2018). Picard Toolkit GitHub Repository: Broad Institute. Retrieved from http://broadinstitute.github.io/picard/
IUCN (International Union for Conservation of Nature). (2016). Equus quagga. The IUCN Red List of Threatened Species. Version 2020-1. Retrieved from https://www.iucnredlist.org/species/41013/45172424
King, S. R. B., & Moehlman, P. D. (2016). Equus quagga. The IUCN Red List of Threatened Species, 2016, e.T41013A45172424. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T41013A45172424.en
Kirin, M., McQuillan, R., Franklin, C. S., Campbell, H., McKeigue, P. M., & Wilson, J. F. (2010). Genomic runs of homozygosity record population history and consanguinity. PLoS One, 5(11), e13996. https://doi.org/10.1371/journal.pone.0013996
Landeau, L., & Terborgh, J. (1986). Oddity and the ‘confusion effect’ in predation. Animal Behavior, 34(5), 1372-1380. https://doi.org/10.1016/S0003-3472(86)80208-1
Larison, B., Harrigan, R. J., Rubenstein, D. I., & Smith, T. B. (2015). Concordance on zebra stripes is not black and white: Response to comment by Caro & Stankowich (2015). Royal Society of Open Science, 2(9), 150359. https://doi.org/10.1098/rsos.150359
Larison, B., Harrigan, R. J., Thomassen, H. A., Rubenstein, D. I., Chan-Golston, A. M., Li, E., & Smith, T. B. (2015). How the zebra got its stripes: A problem with too many solutions. Royal Society of Open Science, 2(1), 140452. https://doi.org/10.1098/rsos.140452
Le Roux, E., Clinnin, G., Druce, D., Owen-Smith, N., Graf, J. A., & Cromsigt, J. P. G. M. (2017). Temporal changes in the large Herbivore Fauna of Hluhluwe-iMfolozi Park. In J. P. G. M. Cromsigt, S. Archibald, & N. Owen-Smith (Eds.), Conserving Africa’s mega-diversity in the anthropocene: The Hluhluwe-iMfolozi park story. Cambridge University Press.
Lee, T.-H., Guo, H., Wang, X., Kim, C., & Paterson, A. H. (2014). SNPhylo: A pipeline to construct a phylogenetic tree from huge SNP data. BMC Genomics, 15(1), 162. https://doi.org/10.1186/1471-2164-15-162
Li, H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv, 1303.3997. http://arxiv.org/abs/1303.3997v2
Ljetoff, M., Folstad, I., Skarstein, F., & Yoccoz, N. G. (2007). Zebra stripes as an amplifier of individual quality? Annales Zoologici Fennici, 44, 368-376.
Lorenzen, E. D., Heller, R., & Siegismund, H. R. (2012). Comparative phylogeography of African savannah ungulates. Molecular Ecology, 21(15), 3656-3670. https://doi.org/10.1111/j.1365-294X.2012.05650.x
Maddock, L. (1979). The “migration” and grazing succession. In A. R. E. Sinclair, & M. Norton-Griffiths (Eds.), Serengetti: Dynamics of an ecosystem (pp. 104-129). University of Chicago Press.
Manichaikul, A., Mychaleckyj, J. C., Rich, S. S., Daly, K., Sale, M., & Chen, W.-M. (2010). Robust relationship inference in genome-wide association studies. Bioinformatics, 26(22), 2867-2873. https://doi.org/10.1093/bioinformatics/btq559
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal, 17(1), 10. https://doi.org/10.14806/ej.17.1.200
Mayr, E. (1982). Of what use are subspecies? The Auk, 99(3), 593-595.
Mayr, E., & Ashlock, P. D. (1991). Principles of systematic biology (2nd ed.). (pp. 475). New York, NY: McGraw-Hill.
McRae, B. H., & Beier, P. (2007). Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National Academy of Sciences of the United States of America, 104(50), 19885-19890. https://doi.org/10.1073/pnas.0706568104
McRae, B. H., Dickson, B. G., Keitt, T. H., & Shah, V. B. (2008). Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology, 89(10), 2712-2724. https://doi.org/10.1890/07-1861.1
Monfort, N. (1977). Observation of a melanistic zebra (Equus burchelli) in the Akagera National Park (Rwanda). African Journal of Ecology, 15, 173.
Moritz, C. (1994). Defining ‘Evolutionarily Significant Units’ for conservation. Trends in Ecology & Evolution, 9(10), 373-375. https://doi.org/10.1016/0169-5347(94)90057-4
Naidoo, R., Chase, M. J., Beytell, P., Du Preez, P., Landen, K., Stuart-Hill, G., & Taylor, R. (2014). A newly discovered wildlife migration in Namibia and Botswana is the longest in Africa. Oryx, 50(1), 138-146. https://doi.org/10.1017/s0030605314000222
Naidoo, R., Kilian, J. W., Du Preez, P., Beytell, P., Aschenborn, O., Taylor, R. D., & Stuart-Hill, G. (2018). Evaluating the effectiveness of local- and regional-scale wildlife corridors using quantitative metrics of functional connectivity. Biological Conservation, 217, 96-103. https://doi.org/10.1016/j.biocon.2017.10.037
O’Brien, S. J., & Mayr, E. (1991). Bureaucratic mischief: Recognizing endangered species and subspecies. Science, 251(4998), 1187-1188.
Oksanen, J., Blanchet, F. G., Kindt, R., & Minchin, P. R. (2018). Vegan: Community ecology package R Package Version 2.5-3.
Pedersen, C.-E., Albrechtsen, A., Etter, P. D., Johnson, E. A., Orlando, L., Chikhi, L., Siegismund, H. R., & Heller, R. (2018). A southern African origin and cryptic structure in the highly mobile plains zebra. Nature Ecology & Evolution, 2(3), 491-498. https://doi.org/10.1038/s41559-017-0453-7
Pemberton, T. J., Absher, D., Feldman, M. W., Myers, R. M., Rosenberg, N. A., & Li, J. Z. (2012). Genomic patterns of homozygosity in worldwide human populations. American Journal of Human Genetics, 91(2), 275-292. https://doi.org/10.1016/j.ajhg.2012.06.014
Phillimore, A. B., & Owens, I. P. (2006). Are subspecies useful in evolutionary and conservation biology? Proceedings of the Royal Society B: Biological Sciences, 273(1590), 1049-1053. https://doi.org/10.1098/rspb.2005.3425
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., & Sham, P. C. (2007). PLINK: A tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81(3), 559-575. https://doi.org/10.1086/519795
Rimmer, A., Phan, H., Mathieson, I., Iqbal, Z., Twigg, S. R. F., WGS500 Consortium, Wilkie, A. O. M., McVean, G., & Lunter, G. (2014). Integrating mapping-, assembly- and haplotype-based approaches for calling variants in clinical sequencing applications. Nature Genetics, 46(8), 912-918. https://doi.org/10.1038/ng.3036
Rowan, J., Kamilar, J. M., Beaudrot, L., & Reed, K. E. (2016). Strong influence of palaeoclimate on the structure of modern African mammal communities. Proceedings of the Royal Society B: Biological Sciences, 283(1840), 20161207. https://doi.org/10.1098/rspb.2016.1207
Ruxton, G. D. (2002). The possible fitness benefits of striped coat coloration for zebra. Mammal Review, 32(4), 237-244. https://doi.org/10.1046/j.1365-2907.2002.00108.x
Stacey, K. (2019). Rare polka-dotted zebra foal photographed in Kenya [Press release]. Retrieved from https://www.nationalgeographic.com/animals/2019/09/zebra-pseudo-melanism-kenya-masai/#:~:text=The%20eye%2Dcatching%20animal%2C%20seen,a%20genetic%20mutation%20called%20pseudomelanism.&text=Talk%20about%20a%20horse%20of,s%20Masai%20Mara%20National%20Reserv
Stoldt, M., Gottert, T., Mann, C., & Zeller, U. (2020). Transfrontier conservation areas and human-wildlife conflict: The case of the Namibian component of the Kavango-Zambezi (KAZA) TFCA. Scientific Reports, 10(1), 7964. https://doi.org/10.1038/s41598-020-64537-9
Thomassen, H. A., Freedman, A. H., Brown, D. M., Buermann, W., & Jacobs, D. K. (2013). Regional differences in seasonal timing of rainfall discriminate between genetically distinct East African giraffe taxa. PLoS One, 8(10), e77191. https://doi.org/10.1371/journal.pone.0077191
Tucker, M. A., Bohning-Gaese, K., Fagan, W. F., Fryxell, J. M., Van Moorter, B., Alberts, S. C., Ali, A. H., Allen, A. M., Attias, N., Avgar, T., Bartlam-Brooks, H., Bayarbaatar, B., Belant, J. L., Bertassoni, A., Beyer, D., Bidner, L., van Beest, F. M., Blake, S., Blaum, N., … Mueller, T. (2018). Moving in the Anthropocene: Global reductions in terrestrial mammalian movements. Science, 359(6374), 466-469. https://doi.org/10.1126/science.aam9712
Wade, C. M., Giulotto, E., Sigurdsson, S., Zoli, M., Gnerre, S., Imsland, F., Lear, T. L., Adelson, D. L., Bailey, E., Bellone, R. R., Distl, O., Edgar, R. C., Garber, M., Leeb, T., Mauceli, E., MacLeod, J. N., Penedo, M. C. T., Raison, J. M., Sharpe, T., … Lindblad-Toh, K. (2009). Genome sequence, comparative analysis, and population genetics of the domestic horse. Science, 326(5954), 865-867. https://doi.org/10.1126/science.1178158
Wang, C., Szpiech, Z. A., Degnan, J. H., Jakobsson, M., Pemberton, T. J., Hardy, J. A., Singleton, A. B., & Rosenberg, N. A. (2010). Comparing spatial maps of human population-genetic variation using Procrustes analysis. Statistical Applications in Genetics and Molecular Biology, 9(1), Article 13.
Wang, C., Zollner, S., & Rosenberg, N. A. (2012). A quantitative comparison of the similarity between genes and geography in worldwide human populations. PLOS Genetics, 8(8), e1002886. https://doi.org/10.1371/journal.pgen.1002886
Waples, R. S., & Anderson, E. C. (2017). Purging putative siblings from population genetic data sets: A cautionary view. Molecular Ecology, 26(5), 1211-1224. https://doi.org/10.1111/mec.14022
Wildlife Conservation Society - WCS Center for International Earth Science Information Network - CIESIN - Columbia University (2005). Last of the Wild Project, Version 2, 2005 (LWP-2): Global Human Influence Index (HII) Dataset (Geographic). Retrieved from https://doi.org/10.7927/H4BP00QC
Zheng, X., Levine, D., Shen, J., Gogarten, S. M., Laurie, C., & Weir, B. S. (2012). A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics, 28(24), 3326-3328. https://doi.org/10.1093/bioinformatics/bts606