Abstract
This study focuses on the taxonomic, evolutionary and conservation implications of a striking reduction in body size previously observed in an island population of gazelles by comparing the genetic structure of island and mainland populations. Mitochondrial sequence diversity of the mainland population was found to be comparable to that of other true gazelles of East Africa. We discuss this in the context of the prolonged armed conflict in our study region. In contrast, the gazelles on Dahlak Kebir, one of the over 200 islands and islets of the Dahlak archipelago on the Red Sea, were found to be genetically depauperate. Nucleotide and haplotype diversity estimates were a sixth and a third of that of the mainland population respectively. Using estimates of Tajima’s D statistic, we inferred that the Dahlak population has undergone expansion after a recent bottleneck. A minimum spanning genealogical network of mitochondrial control region sequences produced testable hypotheses on the route and timing of the colonization of Dahlak Kebir by gazelles from the mainland. Our mitochondrial DNA dataset has resolved the taxonomic ambiguity of the island gazelles. Their genetic distinctiveness and, their striking conformity to the Island Rule that was highlighted in a previous study, are discussed from evolutionary and conservation perspectives.
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References
Arctander P, Kat PW, Aman RA and Siegismund HR (1996) Extreme genetic differences among populations of Gazella granti, Grant's gazelle, in Kenya. Heredity 76: 465–475
Ashton KG, Feldman CR (2003) Bergmann’s rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57:1151–1163
Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Bolton M (1973) Notes on the current status and distribution of some large mammals in Ethiopia (excluding Eritrea). Mammalia 37:562–586
Boom R, Sol CJA, Salismans MMM, Jansen CL, Wertheim-van Dillen PME, van der Noordaa J (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28:495–503
Brisbin ILJ, Geiger RA, Graves HB, Pinder JE III, Sweeney JM, Sweeney JR (1977) Morphological characterizations of two populations of feral swine. Acta Theriol 22:75–85
Brown P, Sutikna T, Morwood MJ, Soejono RP, Jatmiko, Saptomo EW, Due RA (2004) A new small-bodied hominin from the Late Pleistocene of Flores. Indonesia Nature 431:1055–1061
Chiozzi G, Bardelli G, Ricci M, De Marchi G, Cardini A (2014) Just another island dwarf? Phenotypic distinctiveness in the poorly known Soemmerring’s gazelle, Nanger soemmerringii (Cetartiodactyla: Bovidae), of Dahlak Kebir Island. Biol J Linn Soc 111:603–620. https://doi.org/10.1111/bij.12239
Clegg SM, Owens IPF (2002) The ‘island rule’ in birds: medium body size and its ecological explanation. Proc R Soc B Biol Sci 269:1359–1365. https://doi.org/10.1098/rspb.2002.2024
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Eggert LS, Rasner CA, Woodruff DS (2008) The evolution and phylogeography of the African elephant inferred from mitochondrial DNA sequence and nuclear microsatellite markers. Hung Q 49:1993–2006. https://doi.org/10.1098/rspb.2002.2070
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Foster JB (1964) The evolution of mammals on islands. Nature 202:234–235
Gaynor KM, Fiorella KJ, Gregory GH, Kurz DJ, Seto KL, Withey LS, Brashares JS (2016) War and wildlife: linking armed conflict to conservation. Front Ecol Environ 14:533–542. https://doi.org/10.1002/fee.1433
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp 41:95–98
Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920. https://doi.org/10.1093/molbev/msp296
IUCN SSC Antelope Specialist Group (2016) Nanger soemmerringii. The IUCN Red List of Threatened Species 2016: e.T63541A50197739. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T63541A50197739.en. Accessed 31 Jan 2020
Kingdon J (1997) The Kingdon field guide to African mammals. Academic Press, London
Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablancatt FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A 86:6196–6200. https://doi.org/10.1073/2Fpnas.86.16.6196
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Kurihara N, Sin-Ichiro K (2013) Inconsistencies between morphological and genetic subspecies of Grant’s gazelle (Nanger granti). Asian J Anim Vet Adv 8:683–690
Larkin MA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Leigh JW, Bryant D, Nakagawa S (2015) Popart: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210x.12410
Lokatis S, Jeschke JM (2018) The island rule: an assessment of biases and research trends. J Biogeogr 45:289–303. https://doi.org/10.1111/jbi.13160
Lomolino MV (2005) Body size evolution in insular vertebrates: generality of the island rule. J Biogeogr 32:1683–1699. https://doi.org/10.1111/j.1365-2699.2005.01314.x
Lomolino MV, Van der Geer AA, Lyras GA, Palombo MR, Sax DF, Rozzi R (2013) Of mice and mammoths: Generality and antiquity of the island rule. J Biogeogr 40:1427–1439. https://doi.org/10.1111/jbi.12096
Lorenzen ED, Arctander P, Siegismund HR (2008) Three reciprocally monophyletic mtDNA lineages elucidate the taxonomic status of Grant’s gazelles. Conserv Genet 9:593–601. https://doi.org/10.1007/s10592-007-9375-2
Lorenzen ED, Heller R, Siegismund HR (2012) Comparative phylogeography of African savannah ungulates. Mol Ecol 21:3656–3670. https://doi.org/10.1111/j.1365-294X.2012.05650.x
Masseti M, De Marchi G, Chiozzi G (2015) Forbidden islands. The absence of endemics among the insular non-volant terrestrial mammalian fauna of the Red Sea. Nat Hist Sci:2. https://doi.org/10.4081/nhs.2015.253
Meiri S, Cooper N, Purvis A (2008) The island rule: made to be broken? Proc R Soc B 275:141–148. https://doi.org/10.1098/rspb.2007.1056
Millien V (2006) Morphological evolution is accelerated among island mammals. PLoS Biol 4:e321. https://doi.org/10.1371/journal.pbio.0040321
Muwanika VB, Nyakaana S, Siegismund HR (2005) Genetic consequences of war and social strife in sub-Saharan Africa: the case of Uganda’s large mammals. Afr Zool 40:107–113
Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896
Raia P, Meiri S (2006) The island rule in large mammals: paleontology meets ecology. Evolution 60:1731–1742
Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Senn H et al (2014) Splitting or lumping? A conservation dilemma exemplified by the critically endangered dama gazelle (Nanger dama). PLoS ONE 9. https://doi.org/10.1371/journal.pone.0098693
Silva TL, Godinho R, Castro D, Abáigar T, Brito JC, Alves PC (2015) Genetic identification of endangered North African ungulates using noninvasive sampling. Mol Ecol Resour 15:652–661. https://doi.org/10.1111/1755-0998.12335
Steiner CC, Charter SJ, Goddard N, Davis H, Brandt M, Houck ML, Ryder OA (2015) Chromosomal variation and perinatal mortality in San Diego zoo Soemmerring’s gazelles. Zoo Biology 34:374–384. https://doi.org/10.1002/zoo.21223
Tajima F (1989a) The effect of change in population size on DNA polymorphism. Genetics 123:597–601
Tajima F (1989b) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Van der Geer AA, Lyras GA, Lomolino MV, Palombo MR, Sax DF (2013) Body size evolution of palaeo-insular mammals: Temporal variations and interspecific interactions. J Biogeogr 40:1440–1450. https://doi.org/10.1111/jbi.12119
Van Valen L (1973) A new evoultionary law. Evolutionary Theory 30:1–30
Van Vuren DH, Bakker VJ (2009) Rapid morphological change in an insular population of feral sheep. J Zool 277:221–231. https://doi.org/10.1111/j.1469-7998.2008.00531.x
Wilson DE, Reeder DM (2005) Mammal species of the world. A taxonomic and geographic reference, Third. edn. Johns Hopkins University Press, Baltimore
Woolley SM, Posada D, Crandall KA (2008) A comparison of phylogenetic network methods using computer simulation. PLoS ONE:3. https://doi.org/10.1371/journal.pone.0001913
Yalden DW, Largen MJ, Kock D, Hillman JC (1996) Catalogue of the mammals of Ethiopia and Eritrea. 7. Revised checklist, zoogeography and conservation. Tropical Zoology 9:73–164. https://doi.org/10.1080/03946975.1996.10539304
Acknowledgments
We thank the following officials of the Government of the State of Eritrea for issuing us with fieldwork permits and enthusiastically supporting this research. Mr. Arefaine Berhe, Minister of Agriculture; the late Ms. Tsigereda Woldegiorgis, former governor of Northern Red Sea region; and the administrators and staff of the Dahlak sub-region. We are grateful to the Dahlakis who shared with us their knowledge and folktales about the history of gazelles on their island and to the staff of the Division of Wildlife Conservation in the Ministry of Agriculture for assistance in collecting and shipping fecal samples. The data analysis we reported was carried out during KMI’s sabbatical leave affiliation with the Department of Zoology at the University of Khartoum. KMI thanks his hosts Dr. Sumaia Abukashawa and Dr. Mohammed Rahoum.
Funding
This research was supported by a grant to KMI from the National Geographic Committee for Research and Exploration (Grant Number 7967-06).
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Ibrahim, K.M., Williams, P.C., Olson, A. et al. Genetic variation in morphologically divergent mainland and island populations of Soemmerring’s gazelles (Nanger soemmerringii). Mamm Res 65, 403–412 (2020). https://doi.org/10.1007/s13364-020-00480-4
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DOI: https://doi.org/10.1007/s13364-020-00480-4