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Variance in Female Reproductive Success Differentially Impacts Effective Population Size in the Short-Nosed Fruit Bat, Cynopterus sphinx

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Abstract

Effective population size (N e) quantifies the effects of micro-evolutionary processes and the rate of loss of genetic diversity in a population. Several demographic and mating parameters reduce N e. Theoretical studies elucidate the impacts of various demographic and mating system parameters on N e, while empirical studies illustrate realized N e for species with differing life histories and mating systems. However, effect of intra-specific variation in mating system on effective size remains largely unexplored. In this paper we investigated the effect of promiscuous and polygynous mating on N e in two wild populations of the short-nosed fruit bat, Cynopterus sphinx. N e/N (ratio of effective population size to census size) was lower than unity in both populations, and much lower for the polygynous population compared to promiscuous population. Elasticity analyses reveal that N e/N was sensitive to deviations in the sex ratio. Variance in female reproductive success had a higher impact on N e compared to variance in male reproductive success in the promiscuous population. However, for the polygynous population, impact of variance in male reproductive success on N e was higher than that of variance in female reproductive success. Our results suggest that depending on mating system, different populations of the same species could have alternate evolutionary trajectories. The rate of loss of genetic diversity would be lower for the promiscuous population compared to the polygynous population. Our study is the first to highlight which parameters would most significantly impact population specific N e under different mating systems.

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Abbreviations

Ne :

Effective population size

N:

Census population size

r:

Sex ratio, expressed as proportion of males

T:

Mean generational interval

Ai :

Average adult life span for each sex i (i = m: males and i = f: females)

IAi :

Standardized variance in adult life span for for each sex i (i = m: males and i = f: females)

Ibf :

Standardized variance in female fecundity per breeding season

Ibm :

Standardized variance in male mating success per breeding season

vi :

Annual adult survivorship

References

  • Anthony, L. L., & Blumstein, D. T. (2000). Integrating behaviour into wildlife conservation: The multiple ways that behaviour can reduce Ne. Biological Conservation, 95, 303–315.

    Article  Google Scholar 

  • Bateson, P. P. G. (1983). Mate choice. Cambridge: Cambridge University Press.

    Google Scholar 

  • Belmar-Lucero, S., Wood, J. L., Scott, S., Harbicht, A. B., Hutchings, J. A., & Fraser, D. J. (2012). Concurrent habitat and life history influences on effective/census population size ratios in stream dwelling trout. Ecology and Evolution, 2, 562–573.

    Article  PubMed  PubMed Central  Google Scholar 

  • Borkowska, A. (2011). Seasonal variation of reproductive success under female philopatry and male-biased dispersal in a common vole population. Behavioural Processes, 86, 39–45.

    Article  PubMed  Google Scholar 

  • Bouteiller, C., & Perrin, N. (2000). Individual reproductive success and effective population size in the greater white-toothed shrew Crocidura russula. Proceedings of the Royal Society London B, 267, 701–705.

    Article  CAS  Google Scholar 

  • Caballero, A. (1994). Developments in the prediction of effective population size. Heredity, 73, 657–679.

    Article  PubMed  Google Scholar 

  • Clutton-Brock, T. H., Hodge, S. J., Spong, G., Russell, A. F., Jordan, N. R., Bennett, N. C., et al. (2006). Intrasexual competition and sexual selection in cooperative mammals. Nature, 444, 1065–1068.

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock, T. H., & Iason, G. R. (1986). Sex ratio variation in mammals. The Quaterly Review of Biology, 61, 339–374.

    Article  CAS  Google Scholar 

  • Creel, S. (1998). Social organization and effective population size in carnivores. In T. Caro (Ed.), Behavioral ecology and conservation biology (pp. 246–265). New York: Oxford University Press.

    Google Scholar 

  • Cutrera, A. P., Lacey, E. A., & Busch, C. (2006). Intraspecific variation in effective population size in talar tuco-tucos (Ctenomys talarum): The role of demography. Journal of Mammalogy, 87, 108–116.

    Article  Google Scholar 

  • Dirzo, R., Young, H. S., Galetti, M., Ceballos, G., Isaac, N. J., & Collen, B. (2014). Defaunation in the Anthropocene. Science, 345, 401–406.

    Article  CAS  PubMed  Google Scholar 

  • Frankham, R. (1995). Effective population size/adult population size ratios in wildlife: A review. Genetics Research, 66, 95–107.

    Article  Google Scholar 

  • Garg, K. M., Chattopadhyay, B., Swami Doss, P. D., Kumar Vinoth, A., Kandula, S., & Ramakrishnan, U. (2012). Promiscuous mating in the harem-roosting fruit bat, Cynopterus sphinx. Molecular Ecology, 21, 4093–4105.

    Article  PubMed  Google Scholar 

  • Garg, K. M., Chattopadhyay, B., Swami Doss, P. D., Kumar Vinoth, A., Kandula, S., & Ramakrishnan, U. (2015). Males and females gain differentially from sociality in a promiscuous fruit bat Cynopterus sphinx. PLoS One, 10, e0122180.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamilton, M. (2011). Population genetics. New York: Wiley.

    Google Scholar 

  • Harris, R. B., & Allendorf, F. W. (1989). Genetically effective population size of large mammals: An assessment of estimators. Conservation Biology, 3(2), 181–191.

    Article  Google Scholar 

  • Hill, W. G. (1972). Effective size of populations with overlapping generations. Theoretical Population Biology, 3(3), 278–289.

    Article  CAS  PubMed  Google Scholar 

  • Holekamp, K., & Engh, A. L. (2009). Reproductive skew in female. In R. Hager & C. B. Jones (Eds.), Reproductive skew in vertebrates: Proximate and ultimate causes (pp. 53). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Holleley, C. E., Dickman, C. R., Crowther, M. S., & Oldroyd, B. P. (2006). Size breeds success: Multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii. Molecular Ecology, 15, 3439–3448.

    Article  CAS  PubMed  Google Scholar 

  • Kaeuffer, R., Pontier, D., Devillard, S., & Perrin, N. (2004). Effective size of two feral domestic cat populations (Felis catus L.): Effect of the mating system. Molecular Ecology, 13, 483–490.

    Article  CAS  PubMed  Google Scholar 

  • Kraaijeveld-Smit, F. J. L., Ward, S. J., & Temple-Smith, P. D. (2003). Paternity success and the direction of sexual selection in a field population of a semelparous marsupial, Antechinus agilis. Molecular Ecology, 12, 475–484.

    Article  CAS  PubMed  Google Scholar 

  • Lande, R., & Barrowclough, G. F. (1987). Effective population size, genetic variation, and their use in population management. In Viable populations for conservation (pp. 87–123). Cambridge: Cambridge University Press

    Chapter  Google Scholar 

  • Lott, D. F. (1991). Intraspecific variation in the social systems of wild vertebrates, (Vol. 2). Cambridge: Cambridge University Press.

    Google Scholar 

  • Nunney, L. (1993). The influence of mating system and overlapping generations on effective population size. Evolution, 1329–1341.

  • Nunney, L., & Elam, D. R. (1994). Estimating the effective population size of conserved populations. Conservation Biology, 8, 175–184.

    Article  Google Scholar 

  • Palstra, F. P., & Ruzzante, D. E. (2008). Genetic estimates of contemporary effective population size: What can they tell us about the importance of genetic stochasticity for wild population persistence? Molecular Ecology, 17(15), 3428–3447.

    Article  PubMed  Google Scholar 

  • Parker, P. G., & Waite, T. A. (1997). Mating systems, effective population size, and conservation of natural populations. In J. R. Clemmons & R. Buchholz (Eds.), Behavioral approaches to conservation in the wild (pp. 243–261). Cambridge: Cambridge University Press.

    Google Scholar 

  • Ramakrishnan, U. (2002). Conservation genetics of long-lived mammal populations: Applications of individual-based models. San Diego: University of California.

    Google Scholar 

  • Rubenstein, D. I., & Nuñez, C. M. (2009). Sociality and reproductive skew in horses and zebras. In R. Hager & C. B. Jones (Eds.), Reproductive skew in vertebrates: Proximate and ultimate causes (pp. 196–226). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Ruzzante, D. E., McCracken, G. R., Parmelee, S., Hill, K., Corrigan, A., MacMillan, J., et al. (2016). Effective number of breeders, effective population size and their relationship with census size in an iteroparous species, Salvelinus fontinalis. Proceedings of the Royal Society B: Biological Sciences, 283, 20152601.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulte-Hostedde, A. I., & Millar, J. S. (2004). Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): Implications for sperm competition and reproductive success. Behavioral Ecology and Sociobiology, 55, 272–277.

    Article  Google Scholar 

  • Storz, J. F., Bhat, H. R., & Kunz, T. H. (2000). Social structure of a polygynous Tent-making bat, Cynopterus sphinx (Megachiroptera). Journal of Zoology, 251, 151–165.

    Article  Google Scholar 

  • Storz, J. F., Bhat, H. R., & Kunz, T. H. (2001). Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. II. Variance in male mating success and effective population size. Evolution, 55, 1224–1232.

    Article  CAS  PubMed  Google Scholar 

  • Storz, J. F., Ramakrishnan, U., & Alberts, S. C. (2002). Genetic effective size of a wild primate population: Influence of current and historical demography. Evolution, 56, 817–829.

    Article  PubMed  Google Scholar 

  • Wang, J. (2005). Estimation of effective population sizes from data on genetic markers. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 360(1459), 1395–1409.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, J. (2009). A new method for estimating effective population sizes from a single sample of multilocus genotypes. Molecular Ecology, 18, 2148–2164.

    Article  PubMed  Google Scholar 

  • Waples, R. S. (1989). A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics, 121(2), 379–391.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waples, R. S. (2005). Genetic estimates of contemporary effective population size: To what time periods do the estimates apply? Molecular Ecology, 14(11), 3335–3352.

    Article  CAS  PubMed  Google Scholar 

  • Waples, R. S., Do, C., & Chopelet, J. (2011). Calculating Ne and Ne/N in age-structured populations: A hybrid Felsenstein-Hill approach. Ecology, 92(7), 1513–1522.

    Article  PubMed  Google Scholar 

  • Wood, J. W. (1987). The genetic demography of the Gainj of Papua New Guinea. 2. Determinants of effective population size. American Naturalist, 129, 165–187.

    Article  Google Scholar 

  • Wright, S. (1931). Evolution in Mendelian populations. Genetics, 16, 97.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Author acknowledge Vanitha for help with partial derivatives; Balaji for comments on the previous version of the manuscript; Sripathi, DP SwamiDoss, Balaji, Vinoth, Sandeep, Pilot, Venkatesh, Pooja, Megha, Arindam, Madhusmita, Prerona, Debyan, Arjit, Avik, Subhajit, Shivaraj and Dhanabalan for their help in fieldwork.

Author Contributions

KMG conceived the idea, designed the workflow, carried out the lab work, performed all analyses and drafted the final manuscript; UR participated in research design and helped in drafting of the manuscript. All authors read and approved the final version of the manuscript.

Funding

This work was supported by National Centre for Biological Sciences-Tata Institute of Fundamental Research and DST grant (SR/S0/AS-65/2012) (to UR).

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Correspondence to Kritika M. Garg.

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Garg, K.M., Ramakrishnan, U. Variance in Female Reproductive Success Differentially Impacts Effective Population Size in the Short-Nosed Fruit Bat, Cynopterus sphinx . Evol Biol 44, 366–373 (2017). https://doi.org/10.1007/s11692-017-9414-y

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