Mate choice explains high genetic diversity in a small founding population of the New Zealand sea lion (Phocarctos hookeri)
Imogen Foote
A , Stephanie S. Godfrey A and Bruce C. Robertson A B
+ Author Affiliations
- Author Affiliations
A Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand.
B Corresponding author. Email: bruce.robertson@otago.ac.nz
Australian Journal of Zoology 66(6) 343-351 https://doi.org/10.1071/ZO19023
Submitted: 3 April 2019 Accepted: 7 June 2019 Published: 26 June 2019
Abstract
Founder populations are susceptible to reduced genetic diversity, which can hinder successful population establishment. A new genetic lineage of the New Zealand sea lion (Phocarctos hookeri) has recently colonised the historical range of the New Zealand mainland (Otago Peninsula). Despite a small founding population, previous research indicated that nuclear genetic diversity in the Otago Peninsula population is similar to that of the larger source population (Sandy Bay, Auckland Islands). Our research aimed to identify whether mechanisms of female mate choice could help to explain the unexpectedly high level of genetic diversity in the founder population. We used genetic data at 12 microsatellite loci for mother–pup pairs from both populations, and the software COLONY to identify putative paternal genotypes inferred from allele sharing between known mother–pup pairs. We found that mating pairs were, on average, more related at the Otago Peninsula location. However, Sandy Bay females were mating with males more related to themselves than expected by chance, while the Otago Peninsula females were not. These findings suggest that female choice in this otariid species appears important, although may be constrained in some situations. Our findings also help to explain how the recently founded population is able to maintain a viable, growing population.
Additional keywords: mammal, mating system, Otariidae, polygyny, population viability, range expansion.
References
Acevedo-Whitehouse, K., Gulland, F., Greig, D., and Amos, W. (2003). Inbreeding: disease susceptibility in California sea lions. Nature 422, 35.| Inbreeding: disease susceptibility in California sea lions.Crossref | GoogleScholarGoogle Scholar | 12621424PubMed |
Acevedo-Whitehouse, K., Spraker, T. R., Lyons, E., Melin, S. R., Gulland, F., Delong, R. L., and Amos, W. (2006). Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Molecular Ecology 15, 1973–1982.
| Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups.Crossref | GoogleScholarGoogle Scholar | 16689912PubMed |
Augé, A. A., Robertson, B. C., Chilvers, B. L., Mathieu, R., and Moore, A. (2009). Aggregation and dispersion of female New Zealand sea lions at the Sandy Bay breeding colony, Auckland Islands: how unusual is their spatial behaviour? Behaviour 146, 1287–1311.
| Aggregation and dispersion of female New Zealand sea lions at the Sandy Bay breeding colony, Auckland Islands: how unusual is their spatial behaviour?Crossref | GoogleScholarGoogle Scholar |
Bartholomew, G. (1970). A model for the evolution of pinniped polygyny. Evolution 24, 546–559.
| A model for the evolution of pinniped polygyny.Crossref | GoogleScholarGoogle Scholar | 28562995PubMed |
Bejder, L., Fletcher, D., and Bräger, S. (1998). A method for testing association patterns of social animals. Animal Behaviour 56, 719–725.
| A method for testing association patterns of social animals.Crossref | GoogleScholarGoogle Scholar | 9784222PubMed |
Bodkin, J. L., Ballachey, B. E., Cronin, M. A., and Scribner, K. T. (1999). Population demographics and genetic diversity in remnant and translocated populations of sea otters. Conservation Biology 13, 1378–1385.
| Population demographics and genetic diversity in remnant and translocated populations of sea otters.Crossref | GoogleScholarGoogle Scholar |
Brown, D. J., Ribic, C. A., Donner, D. M., Nelson, M. D., Bocetti, C. I., and Deloria-Sheffield, C. M. (2017). Using a full annual cycle model to evaluate long-term population viability of the conservation-reliant Kirtland’s warbler after successful recovery. Journal of Applied Ecology 54, 439–449.
| Using a full annual cycle model to evaluate long-term population viability of the conservation-reliant Kirtland’s warbler after successful recovery.Crossref | GoogleScholarGoogle Scholar |
Campagna, C., and Le Boeuf, B. (1988). Reproductive behaviour of southern sea lions. Behaviour 104, 233–261.
| Reproductive behaviour of southern sea lions.Crossref | GoogleScholarGoogle Scholar |
Campagna, C., Bisioli, C., Quintana, F., and Vila, A. (1992). Group breeding in sea lions: pups survive better in colonies. Animal Behaviour 43, 541–548.
| Group breeding in sea lions: pups survive better in colonies.Crossref | GoogleScholarGoogle Scholar |
Cassini, M. H. (2000). A model of female breeding dispersion and the reproductive systems of pinnipeds. Behavioural Processes 51, 93–99.
| A model of female breeding dispersion and the reproductive systems of pinnipeds.Crossref | GoogleScholarGoogle Scholar | 11074314PubMed |
Caudron, A. K., Negro, S. S., Fowler, M., Boren, L., Poncin, C., Robertson, B. C., and Gemmell, N. J. (2009). Alternative mating tactics in the New Zealand fur seal Arctocephalus forsteri: when non-territorial males are successful too. Australian Journal of Zoology 57, 409–421.
| Alternative mating tactics in the New Zealand fur seal Arctocephalus forsteri: when non-territorial males are successful too.Crossref | GoogleScholarGoogle Scholar |
Charlesworth, D., and Charlesworth, B. (1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18, 237–268.
| Inbreeding depression and its evolutionary consequences.Crossref | GoogleScholarGoogle Scholar |
Chilvers, B. L., and Meyer, S. (2017). Conservation needs for the endangered New Zealand sea lion. Phocarctos hookeri. Aquatic Conservation 27, 846–855.
| Conservation needs for the endangered New Zealand sea lion. Phocarctos hookeri.Crossref | GoogleScholarGoogle Scholar |
Chilvers, B. L., and Wilkinson, I. S. (2008). Philopatry and site fidelity of New Zealand sea lions (Phocarctos hookeri). Wildlife Research 35, 463–470.
| Philopatry and site fidelity of New Zealand sea lions (Phocarctos hookeri).Crossref | GoogleScholarGoogle Scholar |
Chilvers, L., Robertson, B. C., Wilkinson, I. S., Duignan, P. J., and Gemmell, N. J. (2005). Male harassment of female New Zealand sea lions, Phocarctos hookeri: mortality, injury, and harassment avoidance. Canadian Journal of Zoology 83, 642–648.
| Male harassment of female New Zealand sea lions, Phocarctos hookeri: mortality, injury, and harassment avoidance.Crossref | GoogleScholarGoogle Scholar |
Clutton-Brock, T., and Harvey, P. (1978). Mammals, resources and reproductive strategies. Nature 273, 191–195.
| Mammals, resources and reproductive strategies.Crossref | GoogleScholarGoogle Scholar | 347308PubMed |
Clutton-Brock, T., and McAuliffe, K. (2009). Female mate choice in mammals. The Quarterly Review of Biology 84, 3–27.
| Female mate choice in mammals.Crossref | GoogleScholarGoogle Scholar | 19326786PubMed |
Collins, C. J., Rawlence, N. J., Prost, S., Anderson, C. N. K., Knapp, M., Scofield, R. P., Robertson, B. C., Smith, I., Matisoo-Smith, E. A., and Chilvers, B. L. (2014). Extinction and recolonization of coastal megafauna following human arrival in New Zealand. Proceedings of the Royal Society of London. Series B, Biological Sciences 281, 20140097.
| Extinction and recolonization of coastal megafauna following human arrival in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Collins, C. J., Chilvers, B. L., Taylor, M., and Robertson, B. C. (2016). Historical population size of the threatened New Zealand sea lion Phocarctos hookeri. Journal of Mammalogy 97, 436–443.
| Historical population size of the threatened New Zealand sea lion Phocarctos hookeri.Crossref | GoogleScholarGoogle Scholar |
Collins, C., Chilvers, B., Osborne, A., Taylor, M., and Robertson, B. (2017). Unique and isolated: population structure has implications for management of the endangered New Zealand sea lion. Conservation Genetics 18, 1177–1189.
| Unique and isolated: population structure has implications for management of the endangered New Zealand sea lion.Crossref | GoogleScholarGoogle Scholar |
Davidian, E., Courtiol, A., Wachter, B., Hofer, H., and Honer, O. P. (2016). Why do some males choose to breed at home when most other males disperse? Science Advances 2, e1501236.
| Why do some males choose to breed at home when most other males disperse?Crossref | GoogleScholarGoogle Scholar | 27034982PubMed |
de Bruyn, P. J. N., Tosh, C. A., Bester, M. N., Cameron, E. Z., Mcintyre, T., and Wilkinson, I. S. (2011). Sex at sea: alternative mating system in an extremely polygynous mammal. Animal Behaviour 82, 445–451.
| Sex at sea: alternative mating system in an extremely polygynous mammal.Crossref | GoogleScholarGoogle Scholar |
Eberle, M., and Kappeler, P. M. (2004). Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behavioral Ecology and Sociobiology 57, 91–100.
| Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus).Crossref | GoogleScholarGoogle Scholar |
Ellegren, H. (1999). Inbreeding and relatedness in Scandinavian grey wolves Canis Lupus. Hereditas 130, 239–244.
| Inbreeding and relatedness in Scandinavian grey wolves Canis Lupus.Crossref | GoogleScholarGoogle Scholar | 10509138PubMed |
Ellegren, H., and Sheldon, B. (2008). Genetic basis of fitness differences in natural populations. Nature 452, 169–175.
| Genetic basis of fitness differences in natural populations.Crossref | GoogleScholarGoogle Scholar | 18337813PubMed |
Flatz, R., Gonzalez-Suarez, M., Young, J. K., Hernandez-Camacho, C. J., Immel, A. J., and Gerber, L. R. (2012). Weak polygyny in California sea lions and the potential for alternative mating tactics. PLoS One 7, e33654.
| Weak polygyny in California sea lions and the potential for alternative mating tactics.Crossref | GoogleScholarGoogle Scholar | 22432039PubMed |
Frankham, R. (2005). Genetics and extinction. Biological Conservation 126, 131–140.
| Genetics and extinction.Crossref | GoogleScholarGoogle Scholar |
Gales, N. (2009). New Zealand sea lion (Phocarctos hookeri). In ‘Encyclopedia of Marine Mammals’. (Eds W. Perrin, B. Wursig, and J. Thewissen.) pp. 763–765. (Elsevier: USA.)
Gummer, H., Taylor, G., Wilson, K., and Rayner, M. J. (2015). Recovery of the endangered Chatham petrel Pterodroma axillaris: a review of conservation management techniques from 1990 to 2010. Global Ecology and Conservation 3, 310–323.
| Recovery of the endangered Chatham petrel Pterodroma axillaris: a review of conservation management techniques from 1990 to 2010.Crossref | GoogleScholarGoogle Scholar |
Hartnett, C. M., Parrott, M. L., Mulder, R. A., Coulson, G., and Magrath, M. J. L. (2018). Opportunity for female mate choice improves reproductive outcomes in the conservation breeding program of the eastern barred bandicoot (Perameles gunnii). Applied Animal Behaviour Science 199, 67–74.
| Opportunity for female mate choice improves reproductive outcomes in the conservation breeding program of the eastern barred bandicoot (Perameles gunnii).Crossref | GoogleScholarGoogle Scholar |
Hoffman, J. I., and Amos, W. (2005). Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Molecular Ecology 14, 599–612.
| Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion.Crossref | GoogleScholarGoogle Scholar | 15660949PubMed |
Hoffman, J. I., Forcada, J., Trathan, P. N., and Amos, W. (2007). Female fur seals show active choice for males that are heterozygous and unrelated. Nature 445, 912–914.
| Female fur seals show active choice for males that are heterozygous and unrelated.Crossref | GoogleScholarGoogle Scholar | 17287726PubMed |
Horne, T. J., and Ylönen, H. (1996). Female bank voles (Clethrionomys glareolus) prefer dominant males; but what if there is no choice? Behavioral Ecology and Sociobiology 38, 401–405.
| Female bank voles (Clethrionomys glareolus) prefer dominant males; but what if there is no choice?Crossref | GoogleScholarGoogle Scholar |
Jones, O. R., and Wang, J. (2010). COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10, 551–555.
| COLONY: a program for parentage and sibship inference from multilocus genotype data.Crossref | GoogleScholarGoogle Scholar | 21565056PubMed |
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P., and Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |
Kempenaers, B. (2007). Mate choice and genetic quality: a review of the heterozygosity theory. Advances in the Study of Behavior 37, 189–278.
| Mate choice and genetic quality: a review of the heterozygosity theory.Crossref | GoogleScholarGoogle Scholar |
Kirkpatrick, M., and Ryan, M. J. (1991). The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38.
| The evolution of mating preferences and the paradox of the lek.Crossref | GoogleScholarGoogle Scholar |
Kokko, H., and Ots, I. (2006). When not to avoid inbreeding. Evolution 60, 467–475.
| When not to avoid inbreeding.Crossref | GoogleScholarGoogle Scholar | 16637492PubMed |
Lawrence, W. S. (1987). Dispersal: an alternative mating tactic conditional on sex ratio and body size. Behavioral Ecology and Sociobiology 21, 367–373.
| Dispersal: an alternative mating tactic conditional on sex ratio and body size.Crossref | GoogleScholarGoogle Scholar |
Majluf, P., and Goebel, M. E. (1992). The capture and handling of female South American fur seals and their pups. Marine Mammal Science 8, 187–190.
| The capture and handling of female South American fur seals and their pups.Crossref | GoogleScholarGoogle Scholar |
McComb, K. E. (1991). Female choice for high roaring rates in red deer, Cervus elaphus. Animal Behaviour 41, 79–88.
| Female choice for high roaring rates in red deer, Cervus elaphus.Crossref | GoogleScholarGoogle Scholar |
McConkey, S., McConnell, H., Lalas, C., Heinrich, S., Ludmerer, A., McNally, N., Parker, E., Borofsky, C., Schimanski, K., and McIntosh, G. (2002). A northward spread in the breeding distribution of the New Zealand sea lion (Phocarctos Hookeri). Australian Mammalogy 24, 97–106.
| A northward spread in the breeding distribution of the New Zealand sea lion (Phocarctos Hookeri).Crossref | GoogleScholarGoogle Scholar |
McElligott, A. G., Gammell, M. P., Harty, H. C., Paini, D. R., Murphy, D. T., Walsh, J. T., and Hayden, T. J. (2001). Sexual size dimorphism in fallow deer (Dama dama): do larger, heavier males gain greater mating success? Behavioral Ecology and Sociobiology 49, 266–272.
| Sexual size dimorphism in fallow deer (Dama dama): do larger, heavier males gain greater mating success?Crossref | GoogleScholarGoogle Scholar |
Mills, L. S., and Allendorf, F. W. (1996). The one-migrant-per-generation rule in conservation and management. Conservation Biology 10, 1509–1518.
| The one-migrant-per-generation rule in conservation and management.Crossref | GoogleScholarGoogle Scholar |
Ministry for Primary Industries (2017). Aquatic environment and biodiversity annual review 2017. (Ed. Fisheries Science Team) pp. 1–724. (Ministry for Primary Industries: Wellington, New Zealand.)
Mock, K. E., Latch, E. K., and Rhodes, O. E. (2004). Assessing losses of genetic diversity due to translocation: long-term case histories in Merriam’s turkey Meleagris gallopavo merriami. Conservation Genetics 5, 631–645.
| Assessing losses of genetic diversity due to translocation: long-term case histories in Merriam’s turkey Meleagris gallopavo merriami.Crossref | GoogleScholarGoogle Scholar |
Ortega, J., Maldonado, J. E., Wilkinson, G. S., Arita, H. T., and Fleischer, R. C. (2003). Male dominance, paternity, and relatedness in the Jamaican fruit‐eating bat (Artibeus jamaicensis). Molecular Ecology 12, 2409–2415.
| Male dominance, paternity, and relatedness in the Jamaican fruit‐eating bat (Artibeus jamaicensis).Crossref | GoogleScholarGoogle Scholar | 12919478PubMed |
Osborne, A. J., Negro, S. S., Chilvers, B. L., Robertson, B. C., Kennedy, M. A., and Gemmell, N. J. (2016). Genetic evidence of a population bottleneck and inbreeding in the endangered New Zealand sea lion, Phocarctos hookeri. The Journal of Heredity 107, 392–402.
| Genetic evidence of a population bottleneck and inbreeding in the endangered New Zealand sea lion, Phocarctos hookeri.Crossref | GoogleScholarGoogle Scholar | 26995741PubMed |
Peacock, M. M., Beard, K. H., O’Neill, E. M., Kirchoff, V. S., and Peters, M. B. (2009). Strong founder effects and low genetic diversity in introduced populations of Coqui frogs. Molecular Ecology 18, 3603–3615.
| Strong founder effects and low genetic diversity in introduced populations of Coqui frogs.Crossref | GoogleScholarGoogle Scholar | 19674300PubMed |
R Core Team (2017). ‘R: a Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna.)
Reed, D. H., and Frankham, R. (2003). Correlation between fitness and genetic diversity. Conservation Biology 17, 230–237.
| Correlation between fitness and genetic diversity.Crossref | GoogleScholarGoogle Scholar |
Ridgway, S., and Harrison, R. (Eds) (1981). ‘Handbook of Marine Mammals.’ (Academic Press Ltd: London.)
Robertson, B. C., Chilvers, B. L., Duignan, P. J., Wilkinson, I. S., and Gemmell, N. J. (2006). Dispersal of breeding, adult male Phocarctos hookeri: implications for disease transmission, population management and species recovery. Biological Conservation 127, 227–236.
| Dispersal of breeding, adult male Phocarctos hookeri: implications for disease transmission, population management and species recovery.Crossref | GoogleScholarGoogle Scholar |
Sardell, R. J., Kempenaers, B., and Duval, E. H. (2014). Female mating preferences and offspring survival: testing hypotheses on the genetic basis of mate choice in a wild lekking bird. Molecular Ecology 23, 933–946.
| Female mating preferences and offspring survival: testing hypotheses on the genetic basis of mate choice in a wild lekking bird.Crossref | GoogleScholarGoogle Scholar | 24383885PubMed |
Smith, R. H. (1979). On selection for inbreeding in polygynous animals. Heredity 43, 205–211.
| On selection for inbreeding in polygynous animals.Crossref | GoogleScholarGoogle Scholar |
Smuts, B. B., and Smuts, R. W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behavior 22, 1–63.
| Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications.Crossref | GoogleScholarGoogle Scholar |
Sonsthagen, S. A., Coonan, T. J., Latta, B. C., Sage, G. K., and Talbot, S. L. (2012). Genetic diversity of a newly established population of golden eagles on the Channel Islands, California. Biological Conservation 146, 116–122.
| Genetic diversity of a newly established population of golden eagles on the Channel Islands, California.Crossref | GoogleScholarGoogle Scholar |
Spieth, P. T. (1974). Gene flow and genetic differentiation. Genetics 78, 961–965.
| 4452477PubMed |
Szucs, M., Melbourne, B. A., Tuff, T., Weiss-Lehman, C., and Hufbauer, R. A. (2017). Genetic and demongraphic founder effects have long-term fitness consequences for colonising populations. Ecology Letters 20, 436–444.
| Genetic and demongraphic founder effects have long-term fitness consequences for colonising populations.Crossref | GoogleScholarGoogle Scholar | 28145080PubMed |
Taylor, H. R. (2015). The use and abuse of genetic marker-based estimates of relatedness and inbreeding. Ecology and Evolution 5, 3140–3150.
| The use and abuse of genetic marker-based estimates of relatedness and inbreeding.Crossref | GoogleScholarGoogle Scholar | 26357542PubMed |
van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
| Micro-checker: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar |
Vilà, C., Sundqvist, A., Flagstad, Y., Seddon, J., Rnerfeldt, S. B., Kojola, I., Casulli, A., Sand, H., Wabakken, P., and Ellegren, H. (2003). Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proceedings of the Royal Society B: Biological Sciences 270, 91–97.
| Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant.Crossref | GoogleScholarGoogle Scholar | 12590776PubMed |
Waitt, C., Little, A. C., Wolfensohn, S., Honess, P., Brown, A. P., Buchanan-Smith, H. M., and Perrett, D. I. (2003). Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proceedings of the Royal Society B: Biological Sciences 270, 144–146.
| Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice.Crossref | GoogleScholarGoogle Scholar |
Walsh, P. S., Metzger, D. A., and Higuchi, R. (1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10, 506–513.
| 1867860PubMed |
Wang, J. (2007). Triadic IBD coefficients and applications to estimating pairwise relatedness. Genetical Research 89, 135–153.
| Triadic IBD coefficients and applications to estimating pairwise relatedness.Crossref | GoogleScholarGoogle Scholar | 17894908PubMed |
Wang, J. (2011). Coancestry: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Molecular Ecology Resources 11, 141–145.
| Coancestry: a program for simulating, estimating and analysing relatedness and inbreeding coefficients.Crossref | GoogleScholarGoogle Scholar | 21429111PubMed |
Waser, P. M., Austad, S. N., and Keane, B. (1986). When should animals tolerate inbreeding? American Naturalist 128, 529–537.
| When should animals tolerate inbreeding?Crossref | GoogleScholarGoogle Scholar |
White, K. L., Eason, D. K., Jamieson, I. G., and Robertson, B. C. (2015). Evidence of inbreeding depression in the critically endangered parrot, the kakapo. Animal Conservation 18, 341–347.
| Evidence of inbreeding depression in the critically endangered parrot, the kakapo.Crossref | GoogleScholarGoogle Scholar |
Wittmann, M. J., Gabriel, W., and Metzler, D. (2014). Genetic diversity in introduced populations with an Allee effect. Genetics 198, 299–310.
| Genetic diversity in introduced populations with an Allee effect.Crossref | GoogleScholarGoogle Scholar | 25009147PubMed |
Zedrosser, A., Bellemain, E., Taberlet, P., and Swenson, J. E. (2007). Genetic estimates of annual reproductive success in male brown bears: the effects of body size, age, internal relatedness and population density. Journal of Animal Ecology 76, 368–375.
| Genetic estimates of annual reproductive success in male brown bears: the effects of body size, age, internal relatedness and population density.Crossref | GoogleScholarGoogle Scholar | 17302844PubMed |
