全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Determinants and Patterns of Reproductive Success in the Greater Horseshoe Bat during a Population Recovery

DOI: 10.1371/journal.pone.0087199

Full-Text   Cite this paper   Add to My Lib

Abstract:

An individual's reproductive success will depend on traits that increase access to mates, as well as the number of mates available. In most well-studied mammals, males are the larger sex, and body size often increases success in intra-sexual contests and thus paternity. In comparison, the determinants of male success in species with reversed sexual size dimorphism (RSD) are less well understood. Greater horseshoe bats (Rhinolophus ferrumequinum) exhibit RSD and females appear to exert mate choice when they visit and copulate with males in their underground territories. Here we assessed putative determinants of reproductive success in a colony of greater horseshoe bats during a 19-year period of rapid population growth. We genotyped 1080 bats with up to 40 microsatellite loci and assigned maternity to 99.5% of pups, and paternity to 76.8% of pups. We found that in spite of RSD, paternity success correlated positively with male size, and, consistent with our previous findings, also with age. Female reproductive success, which has not previously been studied in this population, was also age-related and correlated positively with individual heterozygosity, but not with body size. Remarkable male reproductive skew was detected that initially increased steadily with population size, possibly coinciding with the saturation of suitable territories, but then levelled off suggesting an upper limit to a male's number of partners. Our results illustrate that RSD can occur alongside intense male sexual competition, that male breeding success is density-dependent, and that male and female greater horseshoe bats are subject to different selective pressures.

References

[1]  Andersson MB (1994) Sexual selection. Chichester: Princeton University Press. 577 p.
[2]  Say L, Naulty F, Hayden TJ (2003) Genetic and behavioural estimates of reproductive skew in male fallow deer. Mol Ecol 12: 2793–2800. doi: 10.1046/j.1365-294x.2003.01945.x
[3]  Clutton-Brock TH, Harvey PH, Rudder B (1977) Sexual dimorphism, socionomic sex-ratio and body-weight in primates. Nature 269: 797–800. doi: 10.1038/269797a0
[4]  Lindenfors P, Tullberg BS, Biuw M (2002) Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behav Ecol Sociobiol 52: 188–193. doi: 10.1007/s00265-002-0507-x
[5]  Spong GF, Hodge SJ, Young AJ, Clutton-Brock TH (2008) Factors affecting the reproductive success of dominant male meerkats. Mol Ecol 17: 2287–2299. doi: 10.1111/j.1365-294x.2008.03734.x
[6]  Hosken DJ (1998) Sperm fertility and skewed paternity during sperm competition in the Australian long-eared bat Nyctophilus geoffroyi (Chiroptera: Vespertilionidae). J Zool 245: 93–100. doi: 10.1111/j.1469-7998.1998.tb00076.x
[7]  Dechmann DKN, Kalko EKV, Konig B, Kerth G (2005) Mating system of a Neotropical roost-making bat: the white-throated, round-eared bat, Lophostoma silvicolum (Chiroptera : Phyllostomidae). Behav Ecol Sociobiol 58: 316–325. doi: 10.1007/s00265-005-0913-y
[8]  Nussey DH, Kruuk LEB, Morris A, Clements MN, Pemberton JM, et al. (2009) Inter- and intrasexual variation in aging patterns across reproductive traits in a wild red deer population. Am Nat 174: 342–357. doi: 10.1086/603615
[9]  Olano-Marin J, Mueller JC, Kempenaers B (2011) Correlations between heterozygosity and reproductive success in the blue tit (Cyanistes caeruleus): an analysis of inbreeding and single locus effects. Evolution 65: 3175–3194. doi: 10.1111/j.1558-5646.2011.01369.x
[10]  Andersson M, Norberg RA (1981) Evolution of reversed sexual size dimorphism and role partitioning among predatory birds, with a size scaling of flight performance. Biol J Linn Soc 15: 105–130. doi: 10.1111/j.1095-8312.1981.tb00752.x
[11]  Monnet JM, Cherry MI (2002) Sexual size dimorphism in anurans. Proc R Soc B 269: 2301–2307. doi: 10.1098/rspb.2002.2170
[12]  Bisazza A, Pilastro A (1997) Small male mating advantage and reversed size dimorphism in poeciliid fishes. J Fish Biol 50: 397–406. doi: 10.1111/j.1095-8649.1997.tb01367.x
[13]  Ralls K (1976) Mammals in which females are larger than males. Quart Rev Biol 51: 245–276. doi: 10.1086/409310
[14]  Schulte-Hostedde AI, Millar JS, Gibbs HL (2004) Sexual selection and mating patterns in a mammal with female-biased sexual size dimorphism. Behav Ecol 15: 351–356. doi: 10.1093/beheco/arh021
[15]  Engh AL, Funk SM, Van Horn RC, Scribner KT, Bruford MW, et al. (2002) Reproductive skew among males in a female-dominated mammalian society. Behav Ecol 13: 193–200. doi: 10.1093/beheco/13.2.193
[16]  Serrano-Meneses MA, Cordoba-Aguilar A, Azpilicueta-Amorin M, Gonzalez-Soriano E, Szekely T (2008) Sexual selection, sexual size dimorphism and Rensch's rule in Odonata. J Evol Biol 21: 1259–1273. doi: 10.1111/j.1420-9101.2008.01567.x
[17]  McLachlan AJ, Allen DF (1987) Male mating success in Diptera - advantages of small size. Oikos 48: 11–14. doi: 10.2307/3565681
[18]  Hernandez MIM, Benson WW (1998) Small-male advantage in the territorial tropical butterfly Heliconius sara (Nymphalidae): a paradoxical strategy? Anim Behav 56: 533–540. doi: 10.1006/anbe.1998.0840
[19]  Raihani G, Szekely T, Serrano-Meneses MA, Pitra C, Goriup P (2006) The influence of sexual selection and male agility on sexual size dimorphism in bustards (Otididae). Anim Behav 71: 833–838. doi: 10.1016/j.anbehav.2005.06.013
[20]  Shine R, Olsson MM, Lemaster MP, Moore IT, Mason RT (2000) Effects of sex, body size, temperature, and location on the antipredator tactics of free-ranging gartersnakes (Thamnophis sirtalis, Colubridae). Behav Ecol 11: 239–245. doi: 10.1093/beheco/11.3.239
[21]  Hodge SJ, Manica A, Flower TP, Clutton-Brock TH (2008) Determinants of reproductive success in dominant female meerkats. J Anim Ecol 77: 92–102. doi: 10.1111/j.1365-2656.2007.01318.x
[22]  Schluter D, Smith JNM (1986) Natural selection on beak and body size in the song sparrow. Evolution 40: 221–231. doi: 10.2307/2408803
[23]  Rughetti M, Festa-Bianchet M (2011) Seasonal changes in sexual size dimorphism in northern chamois. J Zool 284: 257–264. doi: 10.1111/j.1469-7998.2011.00800.x
[24]  Myers P (1978) Sexual dimorphism in size of Vespertilionid bats. Am Nat 112: 701–711. doi: 10.1086/283312
[25]  Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Phil Trans R Soc B 361: 319–334. doi: 10.1098/rstb.2005.1784
[26]  Kervinen M, Alatalo RV, Lebigre C, Siitari H, Soulsbury CD (2012) Determinants of yearling male lekking effort and mating success in black grouse (Tetrao tetrix). Behav Ecol 23: 1209–1217. doi: 10.1093/beheco/ars104
[27]  Szulkin M, Sheldon BC (2008) Dispersal as a means of inbreeding avoidance in a wild bird population. Proc R Soc B 275: 703–711. doi: 10.1098/rspb.2007.0989
[28]  Smith JNM (2006) Conservation and biology of small populations : the song sparrows of Mandarte Island. New York; Oxford: Oxford University Press.
[29]  Part T, Gustafsson L (1989) Breeding dispersal in the collared flycatcher (Ficedula-Albicollis) - possible causes and reproductive consequences. J Anim Ecol 58: 305–320. doi: 10.2307/5002
[30]  Kruuk LEB, Hill WG (2008) Introduction. Evolutionary dynamics of wild populations: the use of long-term pedigree data. Proc R Soc B 275: 593–596. doi: 10.1098/rspb.2007.1689
[31]  Clutton-Brock TH (1982) Red deer: behavior and ecology of two sexes. Chicago: Chicago University Press. 378 p.
[32]  Clutton-Brock TH, Pemberton JM (2004) Soay sheep : dynamics and selection in an island population. Cambridge: Cambridge University Press.
[33]  Goodall J (1986) The chimpanzees of Gombe : patterns of behavior. Cambridge, MA: Harvard University Press.
[34]  Rawlins RG, Kessler MJ (1986) The Cayo Santiago macaques. History, behaviour and biology. Albany, New York: State University of New York Press.
[35]  Ransome RD (1968) The distribution of the greater horse-shoe bat, Rhinolophus ferrumequinum, during hibernation, in relation to environmental factors. J Zool 154: 77–112. doi: 10.1111/j.1469-7998.1968.tb05040.x
[36]  Ransome RD (1989) Population-changes of greater horseshoe bats studied near Bristol over the past 26 years. Biol J Linn Soc 38: 71–82. doi: 10.1111/j.1095-8312.1989.tb01564.x
[37]  Ransome R (1990) The natural history of hibernating bats/London: Christopher Helm. 224 p.
[38]  Rossiter SJ, Ransome RD, Faulkes CG, Dawson DA, Jones G (2006) Long-term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism. Mol Ecol 15: 3035–3043. doi: 10.1111/j.1365-294x.2006.02987.x
[39]  Ransome RD (1991) Greater horseshoe bat. In: Corbet GB HS, editor. The Handbook of British Mammals. Oxford: Blackwell Scientific. pp. 88–94.
[40]  Rossiter SJ, Jones G, Ransome RD, Barratt EM (2000) Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum). Proc R Soc B 267: 545–551. doi: 10.1098/rspb.2000.1035
[41]  Ransome RD (1995) Earlier breeding shortens life in female greater horseshoe bats. Phil Trans R Soc B 350: 153–161. doi: 10.1098/rstb.1995.0149
[42]  Rossiter SJ, Jones G, Ransome RD, Barratt EM (2001) Outbreeding increases offspring survival in wild greater horseshoe bats (Rhinolophus ferrumequinum). Proc R Soc B 268: 1055–1061. doi: 10.1098/rspb.2001.1612
[43]  Rossiter SJ, Burland TM, Jones G, Barratt EM (1999) Characterization of microsatellite loci in the greater horseshoe bat Rhinolophus ferrumequinum. Mol Ecol 8: 1959–1960. doi: 10.1046/j.1365-294x.1999.00778-2.x
[44]  Dawson DA, Rossiter SJ, Jones G, Faulkes CG (2004) Microsatellite loci for the greater horseshoe bat, Rhinolophus ferrumequinum (Rhinolophidae, Chiroptera) and their cross-utility in 17 other bat species. Mol Ecol Notes 4: 96–100. doi: 10.1046/j.1471-8286.2003.00580.x
[45]  Hua PY, Guo TT, Liu WC, Zhang SY, Rossiter S (2009) Isolation and characterization of 13 microsatellite loci in Rhinolophus pusillus (least horseshoe bat) with cross-amplification in five related species. Cons Gen 10: 597–600. doi: 10.1007/s10592-008-9586-1
[46]  Liu WC, Zhang JS, Hua PY, Zhang SY, Rossiter SJ (2009) Development and characterization of novel microsatellite markers from the Chinese rufous horseshoe bat (Rhinolophus sinicus) with cross-species amplification in closely related taxa. Mol Ecol Res 9: 183–185. doi: 10.1111/j.1755-0998.2008.02434.x
[47]  Mao XG, Liu Y, Zhou YY, He BB, Zhang SY (2009) Development of 19 polymorphic microsatellite loci for the intermediate horseshoe bat, Rhinolophus affinis (Rhinolophidae, Chiroptera). Cons Gen 10: 709–711. doi: 10.1007/s10592-008-9625-y
[48]  Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7: 639–655. doi: 10.1046/j.1365-294x.1998.00374.x
[49]  Jones OR, Wang JL (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10: 551–555. doi: 10.1111/j.1755-0998.2009.02787.x
[50]  Walling CA, Pemberton JM, Hadfield JD, Kruuk LEB (2010) Comparing parentage inference software: reanalysis of a red deer pedigree. Mol Ecol 19: 1914–1928. doi: 10.1111/j.1365-294x.2010.04604.x
[51]  Nonacs P (2000) Measuring and using skew in the study of social behavior and evolution. Am Nat 156: 577–589. doi: 10.1086/316995
[52]  Nonacs P (2003) Skew Calculator 2003.
[53]  Strier KB, Chaves PB, Mendes SL, Fagundes V, Di Fiore A (2011) Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate. Proc Natl Acad Sci USA 108: 18915–18919. doi: 10.1073/pnas.1116737108
[54]  Nonacs P (2003) Skew Calculator 2003: Program manual (PDF).
[55]  Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes. R package
[56]  R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.
[57]  Coulon A (2010) GENHET: an easy-to-use R function to estimate individual heterozygosity. Mol Ecol Res 10: 167–169. doi: 10.1111/j.1755-0998.2009.02731.x
[58]  Clutton-Brock TH, Albon SD, Guinness FE (1988) Reproductive success in male and female red deer. In: Clutton-Brock TH, editor. Reproductive success. Chicago: University of Chicago Press. 325–343 p.
[59]  Willisch CS, Biebach I, Koller U, Bucher T, Marreros N, et al. (2012) Male reproductive pattern in a polygynous ungulate with a slow life-history: the role of age, social status and alternative mating tactics. Evol Ecol 26: 187–206. doi: 10.1007/s10682-011-9486-6
[60]  Voigt CC, Heckel G, Mayer F (2005) Sexual selection favours small and symmetric males in the polygynous greater sac-winged bat Saccopteryx bilineata (Emballonuridae, Chiroptera). Behav Ecol Sociobiol 57: 457–464. doi: 10.1007/s00265-004-0874-6
[61]  Hakkarainen H, Korpimaki E (1991) Reversed sexual size dimorphism in Tengmalm owl - is small male size adaptive? Oikos 61: 337–346. doi: 10.2307/3545241
[62]  Gagliardi C, Liukkonen JR, Phillippi-Falkenstein KM, Harrison RM, Kubisch HM (2007) Age as a determinant of reproductive success among captive female rhesus macaques (Macaca mulatta). Reproduction 133: 819–826. doi: 10.1530/rep-06-0323
[63]  Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol 18: 2746–2765. doi: 10.1111/j.1365-294x.2009.04247.x
[64]  Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9: 1013–1027. doi: 10.1046/j.1365-294x.2000.00964.x
[65]  Stevens RD, Johnson ME, McCulloch ES (2013) Absolute and relative secondary-sexual dimorphism in wing morphology: a multivariate test of the ‘Big Mother’ hypothesis. Acta Chiropterol 15: 163–170. doi: 10.3161/150811013x667966
[66]  Ransome RD, McOwat TP (1994) Birth timing and population-changes in greater horseshoe bat colonies (Rhinolophus ferrumequinum) are synchronized by climatic temperature. Zool J Linn Soc 112: 337–351. doi: 10.1111/j.1096-3642.1994.tb00324.x
[67]  Burland TM, Barratt EM, Beaumont MA, Racey PA (1999) Population genetic structure and gene flow in a gleaning bat, Plecotus auritus. Proc R Soc B 266: 975–980. doi: 10.1098/rspb.1999.0732
[68]  McCracken GF, Wilkinson GS (2000) Bat mating systems. In: Crichton EG, Krutzsch PH, editors. Reproductive biology of bats. Cambridge: Academic Press. 321–357 p.
[69]  Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nurnberg P, et al. (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proc R Soc B 271: 819–826. doi: 10.1098/rspb.2003.2666
[70]  Muniz L, Perry S, Manson JH, Gilkenson H, Gros-Louis J, et al. (2010) Male dominance and reproductive success in wild white-faced capuchins (Cebus capucinus) at Lomas Barbudal, Costa Rica. Am J Primatol 72: 1118–1130. doi: 10.1002/ajp.20876
[71]  Isaac JL, Johnson CN (2003) Sexual dimorphism and synchrony of breeding: variation in polygyny potential among populations in the common brushtail possum, Trichosurus vulpecula. Behav Ecol 14: 818–822. doi: 10.1093/beheco/arg076

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133