Abstract
We analysed the diversity of the cytochrome b gene in Iberian ibex (Capra pyrenaica) populations in the southern Iberian Peninsula by sequencing a fragment (987 bp) of this gene in 347 ibex from 10 population nuclei in Andalusia. We found 25 different haplotypes, which account for 64.10% of all haplotypes thus far described for the species (n = 39). All ibex populations other than those from Sierra de Loja shared haplotype EU081020, which was also the most frequent. Twenty haplotypes (80%) were present exclusively in just one population. Of the studied populations, ibex from the Sierra Nevada Natural Space had the greatest genetic diversity in this marker, which was found to harbour 17 cyt b haplotypes. Phylogenetic analyses based on the cytochrome b marker do not support the subspecific classification of this taxon proposed at the beginning of the twentieth century, although three distinct management units can be distinguished. Finally, we discuss the implications of our results on the management of this species. Although the results presented do not describe the structure of the population or the gene flow, it gives an accurate picture of the diversity of this mitochondrial marker, which can be considered a reflection of the historical processes that these populations have undergone.
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References
Acevedo P, Cassinello J, Gortázar C (2007) The Iberian ibex is under an expansion trend but displaced to suboptimal habitats by the presence of extensive goat livestock in central Spain. Biodiv Conserv 16:3361–3376. https://doi.org/10.1007/s10531-006-9032-y
Alados CL (1985) Distribution and status of the Spanish Ibex (Capra pyrenaica). In: Lovari S (ed) The Biology and Management of Mountain Ungulates. Croom-Helm, Beckenham, pp 204–211
Allio R, Donega S, Galtier N, Nabholz B (2017) Large variation in the ratio of mitochondrial to nuclear mutation rate across animals: implications for genetic diversity and the use of mitochondrial DNA as a molecular marker. Mol Biol Evol 34:2762–2772. https://doi.org/10.1093/molbev/msx197
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Angelone-Alasaad S, Biebach I, Pérez JM, Soriguer RC, Granados JE (2017) Molecular analyses reveal unexpected genetic structure in Iberian ibex populations. PLoS ONE 12:e0170827. https://doi.org/10.1371/journal.pone.0170827.s001
Avise JC (2004) Molecular markers: natural history and evolution, 2nd edn. Sinauer Associates Inc, Sunderland, MA
Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A 76(4):1967–1971. https://doi.org/10.1073/pnas.76.4.1967
Burr SP, Pezet M, Chinnery PF (2018) Mitochondrial dna heteroplasmy and purifying selection in the mammalian female germ line. Dev Growth Differ 60(1):21–32. https://doi.org/10.1111/dgd.12420
Cabrera A (1911) The subspecies of the Spanish ibex. Proc Zool Soc Lond 1911:963–967
Cabrera A (1914) Fauna Ibérica. Mamíferos. Museo Nacional de Ciencias Naturales, Madrid
Chen L, Qiu Q, Jiang Y, Wang K, Lin Z, Li Z, Bibi F, Yang Y, Wang J, Nie W, Su W, Liu G, Li Q, Fu W, Pan X, Liu C, Yang J, Zhang C, Yin Y, Wang Y, Zhao Y, Zhang C, Wang Z, Qin Y, Liu W, Wang B, Ren Y, Zhang R, Zeng Y, da Fonseca RR, Wei B, Li R, Wan W, Zhao R, Zhu W, Wang Y, Duan S, Gao Y, Zhang YE, Chen C, Hvilsom C, Epps CW, Chemnick LG, Dong Y, Mirarab S, Siegismund HR, Ryder OA, Gilbert MTP, Lewin HA, Zhang G, Heller R, Wang W (2019) Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits. Science 364(6446):eaav6202. https://doi.org/10.1126/science.aav6202
Chirosa M, Delibes-Senna JR, Fandos P, Granados JE, Pérez MC, Pérez JM, Ruiz-Martínez I, Serrano E, Soriguer RC, Weikam S (2002) Estimas poblacionales de Capra pyrenaica hispanica. In: Pérez JM (ed) Distribución, genética y estatus sanitario de las poblaciones andaluzas de cabra montés. Universidad de Jaén, Junta de Andalucía, Sevilla, Jaén, pp 1–68
Crampe JP, Sourp E, Cavailhes J (2015) Reintroduction du bouquetin ibérique dans les Pyrenees, quand le revedevient reálité. 33èmes Rencontres du GEEFSM, 21–24
Daura J, Sanz M, Julià R, García-Fernández D, Fornos JJ, Vaquero M, Allue E, López-García JM, Blain HA, Ortiz JE, Torres T, Albert RM, Rodríguez-Cintas A, Sánchez-Marco A, Cerdeño E, Skinner AR, Asmeron Y, Polyak VJ, Garces M, Arnold LJ, Demuro M, Pike AWG, Euba I, Rodríguez RF, Yagüe AS, Villaescusa L, Gómez S, Rubio A, Pedro M, Fullola JM, Zilhao J (2015) Cova del Rinoceront (Castelldefels, Barcelona): a terrestrial record for the Last Interglacial period (MIS 5) in the Mediterranean coast of the Iberian Peninsula. Quat Sci Rev 114:203–227. https://doi.org/10.1016/j.quascirev.2015.02.014
Djan M, Maletic V, Trbojevic I, Popovic D, Velickovic N, Burazerovic J, Cirovic D (2014) Genetic diversity and structuring of the grey wolf population from the Central Balkans based on mitochondrial DNA variation. Mammal Biol 79:277–282. https://doi.org/10.1016/j.mambio.2014.03.001
Fonseca C, Migueis D, Fernandes T, Carvalho H, Loureiro A, Carvalho J, Tinoco Torres R (2017) The return of the Iberian wild goat Capra pyrenaica to Portugal: from reintroduction to reconolonization. J Nat Conserv 38:56–61. https://doi.org/10.1016/j.jnc.2017.05.006
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140. https://doi.org/10.1016/j.biocon.2005.05.002
Gebremedhin B, Ficetola GF, Naderi S, Rezaei HR, Maudet C, Rioux D, Luikart G, Flagstad Ø, Thuiller W, Taberlet P (2009a) Frontiers in identifying conservation units: from neutral markers to adaptive genetic variation. Anim Conserv 12:107–109. https://doi.org/10.1111/j.1469-1795.2009.00255.x
Gebremedhin B, Ficetola GF, Naderi S, Rezaei HR, Maudet C, Rioux D, Luikart G, Flagstad Ø, Thuiller W, Taberlet P (2009b) Combining genetic and ecological data to assess the conservation status of the endangered Ethiopian walia ibex. Anim Conserv 12:89–100. https://doi.org/10.1111/j.1469-1795.2009.00238.x
Gonzales G (1982) Eco-ethologie des ongulés de montagne, aproche evolutive. Acta Biol Montana 1:121–152
Granados JE, Soriguer RC, Pérez JM, Fandos P, García-Santiago J (2002) La cabra montés. In: Palomo LJ, Gisbert J (eds), Atlas de los Mamíferos Terrestres de España, pp. 326-329, Madrid
Granados JE, Ros-Candeira A, Pérez-Luque A, Moreno-Llorca R, Cano-Manuel FJ, Fandos P, Soriguer RC, Espinosa Cerrato J, Pérez Jiménez JM, Ramos B, Zamora R (2020) Long-term monitoring of the Iberian ibex population in the Sierra Nevada of the southeast Iberian Peninsula. Sci Data 7:203. https://doi.org/10.1038/s41597-020-0544-1
Grossen C, Biebach I, Angelone-Alasaad S, Keller LF, Croll D (2018) Population genomics analyses of European ibex species show lower diversity and higher inbreeding in reintroduced populations. Evol Appl 11(2):123–139. https://doi.org/10.1111/eva.12490
Grossen C, Guillaume F, Keller LF, Croll D (2020) Purging of highly deleterious mutations through severe bottlenecks in Alpine ibex. Nat Commun 11:1–12. https://doi.org/10.1038/s41467-020-14803-1
Groves C, Grubb P (2011) Ungulate Taxonomy. The Johns Hopkins University Press, Baltimore, MD
Groves P, Shields GF (1996) Phylogenetics of the Caprinae based on cytochrome b sequence. Mol Phylogenet Evol 5:467–476. https://doi.org/10.1006/mpev.1996.0043
Grubb P (2001) Review of family-group names of living bovids. J Mammal 82:374–388. https://doi.org/10.1644/1545-1542(2001)082%3C0374:ROFGNO%3E2.0.CO;2
Haag-Liautard C, Coffe N, Houle D, Lynch M, Charlesworth B, Keightley PD (2008) Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. PLoS Biol 6:e204. https://doi.org/10.1371/journal.pbio.0060204
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Hartl GB, Meneguz PG, Appollonio M, Marco I, Nadlinger K, Suchentrunk F (1992) Molecular systematics of ibex in western Europe. In: Actas del Congreso Internacional del Género Capra en Europa, pp. 21–26, Ronda
Hassanin A, Lecointre G, Tillier S (1998) The ‘evolutionary signal’ of homoplasy in protein-coding gene sequences and its consequences for a priori weighting in phylogeny. C R Acad Sci III 321:611–620. https://doi.org/10.1016/S0764-4469(98)80464-2
Hassanin A, Ropiquet A, Couloux A, Cruaud C (2009) Evolution of the mitochondrial genome in mammals living at high altitude: new insights from a study of the tribe Caprini (Bovidae, Antilopinae). J Mol Evol 68:293–310. https://doi.org/10.1007/s00239-009-9208-7
Hunt SE, McLaren W, Gil L, Thormann A, Schuilenburg H, Sheppard D, Parton A, Armena IM, Trrevanion SJ, Flicek P, Cunningham F (2018) Ensembl variation resources. Database 2018:1–12. https://doi.org/10.1093/database/bay119
IUCN, 2017. The IUCN red list of threatened species. Version 2017–3. <www.iucnredlist.org>. Downloaded on 12 May 2018.
Kazanskaya EY, Kuznetsova MV, Danilkin AA (2007) Phylogenetic reconstructions in the Genus Capra (Bovidae, Artiodactyla) based on the mitochondrial DNA analysis. Genetika 43:245–253. https://doi.org/10.1134/S1022795407020135
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Luo A, Zhang A, Ho SY, Xu W, Zhang Y, Shi W, Cameron SL, Zhu C (2011) Potential efficacy of mitochondrial genes for animal DNA barcoding: a case study using eutherian mammals. BMC Genomics 12(1):84. https://doi.org/10.1186/1471-2164-12-84
Lynch M (2007) The origins of genome architecture. Sinauer, Sunderland
Manceau V, Crampe JP, Boursot P, Taberlet P (1999) Identification of evolutionary significant units in the Spanish wild goat, Capra pyrenaica (Mammalia, Artiodactyla). Anim Conserv 2:33–39. https://doi.org/10.1111/j.1469-1795.1999.tb00046.x
Maudet C, Luikart G, Taberlet P (2001) Development of microsatellite multiplexes for wild goats using primers designed from domestic Bovidae. Genet Sel Evol 33:S193–S203. https://doi.org/10.1186/BF03500880
Moço G, Guerreiro M, Ferreira AF, Rebelo A, Loureiro A, Petrucci-Fonseca F, Pérez JM (2006) The ibex Capra pyrenaica returns to its former Portuguese range. Oryx 40:351–354. https://doi.org/10.1017/S0030605306000718
Morales-Barbero J, Martínez PA, Ferrer-Castán D, Olalla-Tárraga MÁ (2018) Quaternary refugia are associated with higher speciation rates in mammalian faunas of the Western Palaearctic. Ecography 41:607–621. https://doi.org/10.1111/ecog.02647|
Moritz C (1994) Defining “Evolutionarily Significant Units” for conservation. Trends Ecol Evol 9:373–375. https://doi.org/10.1016/0169-5347(94)90057-4
Nieto Feliner G (2011) Southern European glacial refugia: a tale of tales. Taxon 60:365–372. https://doi.org/10.1002/tax.602007|
Ning FY, Fu J, Du ZH (2017) Mitochondrial DNA insertions in the nuclear Capra hircus genome. Genet. Mol. Res. 16:gmr16018266. https://doi.org/10.4238/gmr16018266
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460
Pérez JM, Granados JE, Soriguer RC, Fandos P, Márquez FJ, Crampe JP (2002) Distribution, status and conservation problems of the Spanish Ibex, Capra pyrenaica (Mammalia: Artiodactyla). Mammal Rev 32:26–39. https://doi.org/10.1046/j.1365-2907.2002.00097.x
Pidancier N, Jordan S, Luikart G, Taberlet P (2006) Evolutionary history of the genus Capra (Mammalia, Artiodactyla): Discordance between mitochondrial DNA and Y-chromosome phylogenies. Mol Phylogenet Evol 40:739–749. https://doi.org/10.1016/j.ympev.2006.04.002
Posth C, Wißing C, Kitagawa K, Pagani L, van Holstein L, Racimo F, Wehrberger K, Conard NJ, Kind CJ, Bocherens H, Krause J (2017) Deeply divergent archaic mitochondrial genome provides lower time boundary for African gene flow into Neanderthals. Nat Commun 8:16046. https://doi.org/10.1038/ncomms16046
Pyron RA, Burbrink FT (2013) Phylogenetic estimates of speciation and extinction rates for testing ecological and evolutionary hypotheses. Trends Ecol Evol 28:729–736. https://doi.org/10.1016/j.tree.2013.09.007
Randi E (2000) Mitochondrial DNA. In: Barker AJ (ed) Molecular methods in Ecology. Oxford, UK, pp 136–167
Reed DH, Briscoe DA, Frankham R (2002) Inbreeding and extinction: the effect of environmental stress and lineage. Conserv Genet 3:301–307. https://doi.org/10.1023/A:1019948130263
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Schaller G (1977) Mountain Monarchs. University of Chicago Press, Chicago, IL
Schmitt T, Varga Z (2012) Extra-Mediterranean refugia: the rule and not the exception. Front Zool 9:22. https://doi.org/10.1186/1742-9994-9-22
Song H, Buhay JE, Whiting MF, Crandall KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci U S A 105:13486–13491. https://doi.org/10.1073/pnas.0803076105
Sun MH, Yue CW, Liu TT, Li L, Liu HY (2017) The complete mitochondrial genome of Budorcas taxicolor bedfordi (Artiodactyla: Bovidae) and phylogenetic studies of Caprinae. Conserv Genet Resour 9(3):397–400. https://doi.org/10.1007/s12686-017-0693-5
Turnbaugh PJ, Quince C, Faith JJ, McHardy AC, Yatsunenko T, Niazi F, Affourtit J, Egholm M, Henrissat B, Knight R, Gordon JI (2010) Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Nat Acad Sci 107(16):7503–7508. https://doi.org/10.1073/pnas.1002355107
Ureña I, Arsuaga JL, Galindo-Pellicena MA, Götherström A, Valdiosera C (2011) Filogenia y evolución local de la cabra montés (Capra pyrenaica) en el yacimiento Cuaternario de Chaves (Huesca, España). Bol R Soc Esp Hist Nat Sec Geol 105:5–14
Ureña I, Ersmark E, Samaniego JA, Galindo-Pellicena MA, Cregut-Bonnoure E, Bolivar H, Gómez-Olivencia A, Ríos-Garaizar J, Gárate D, Dalen L, Arsuaga JL, Valdiosera CE (2018) Unraveling the genetic history of the European wild goats. Quat Sci Rev 185:189–198. https://doi.org/10.1016/j.quascirev.2018.01.017
Vilaca ST, Biosa D, Zachos F, Iacolina L, Kirschning J, Alves PC, Paule L, Gortazar C, Mamuris Z, Jedrzejewska B, Borowik T, Sidorovich VE, Kusak J, Costa S, Schley L, Hartl GB, Apollonio M, Bertorelle G, Scandura M (2014) Mitochondrial phylogeography of the European wild boar: the effect of climate on genetic diversity and spatial lineage sorting across Europe. J Biogeogr 41:987–998. https://doi.org/10.1111/jbi.12268
Whitlock MC, Mccauley DE (1999) Indirect measures of gene flow and migration: FST≠ 1/(4Nm+ 1). Heredity 82:117–125. https://doi.org/10.1038/sj.hdy.6884960
Xin W, Yue-Hui MA, Hong C (2006) Analysis of the genetic diversity and the phylogenetic evolution of Chinese sheep based on cyt b gene sequences. Acta Genet Sin 33:1081–1086. https://doi.org/10.1016/S0379-4172(06)60145-5
Yang C, Xiang C, Qi W, Xia S, Tu F, Zhang X, Moermond T, Yue B (2013) Phylogenetic analyses and improved resolution of the family Bovidae based on complete mitochondrial genomes. Biochem Syst Ecol 48:136–143. https://doi.org/10.1016/j.bse.2012.12.005
Yuasa T, Nagata J, Hamasaki S, Tsuruga H, Furubayashi K (2007) The impact of habitat fragmentation on genetic structure of the Japanese sika deer (Cervus nippon) in southern Kantoh, revealed by mitochondrial D-loop sequences. Ecol Res 22:97–106. https://doi.org/10.1007/s11284-006-0190-x
Acknowledgements
The authors wish to thank all those involved in the collection of the samples. This study was funded by an agreement between the Junta de Andalucía (Consejería de Medio Ambiente) and the University of Jaén: Seguimiento y control de la sarna sarcóptica en las poblaciones de cabra montés (C. p. hispanica) existentes en Andalucía. The research activities of the authors are partially funded by the PAIDI (Junta de Andalucía): BIO-294 and RNM-118 groups. The technical and human support provided by Centro de Instrumentación Científico-Técnica (CICT)-Servicios Centrales de Apoyo a la Investigación (SCAI) of Universidad de Jaén (MICINN, Junta de Andalucía, FEDER) is gratefully acknowledged. We thank two anonymous referees for valuable comments on the manuscript.
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Márquez, F.J., Granados, J.E., Caruz, A. et al. Genetic diversity of cytochrome b in Iberian ibex from Andalusia. Mamm Biol 100, 675–684 (2020). https://doi.org/10.1007/s42991-020-00077-z
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DOI: https://doi.org/10.1007/s42991-020-00077-z