Female mate choice in the fat-tailed dunnart (Sminthopsis crassicaudata) influences offspring sex ratio, but not fecundity
Brittney P. Gill
A * , Amy M. Edwards A B C , Marissa L. Parrott D , Emily L. Scicluna A and Kylie A. Robert A E
+ Author Affiliations
- Author Affiliations
A School of Agriculture, Biomedicine & Environment, La Trobe University, Melbourne, Vic. 3086, Australia.
B New South Wales National Parks and Wildlife Service, Bathurst, NSW 2795, Australia.
C University of New England, Armidale, NSW 2350, Australia.
D Wildlife Conservation and Science, Zoos Victoria, Parkville, Vic. 3052, Australia.
E Research Centre for Future Landscapes, La Trobe University, Melbourne, Vic. 3086, Australia.
Australian Journal of Zoology 70(5) 133-141 https://doi.org/10.1071/ZO22028
Submitted: 22 October 2021 Accepted: 21 March 2023 Published: 17 May 2023
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Obtaining a suitable mate is an integral part of reproduction, with sexual selection processes such as female mate choice resulting in both direct and/or indirect benefits. Here, we investigated whether olfactory driven female mate choice influenced reproductive success in captive fat-tailed dunnarts (Sminthopsis crassicaudata). Although females spent 67% more time with a preferred male’s scent, reproductive success was not influenced by assigned mate choice. Of the 10 (of 12) litters that survived to weaning, average litter size was higher for non-preferred pairings (3 ± 0.83) compared with preferred pairings (1.6 ± 0.60), with weaning success equal for both pairings. Analyses suggested that offspring sex ratios were influenced by mate choice, with females paired with their preferred mate having more daughters (81%) in comparison to non-preferred pairings (44%) and by paternal body condition, whereby females paired with males in better body condition produced more sons. In this species, altering offspring sex ratios in favour of daughters may be achieved by pairing with preferred males, and towards sons by pairing with males in better body condition. With the increasing need for captive breeding programs, these techniques may provide opportunities to correct sex ratio biases and incorporate natural mating systems into conservation programs.
Keywords: captive breeding, conservation, dasyurid, female mate choice, life history, marsupial, olfactory cues, reproductive output, sex ratios.
References
Andersson MB (1994) ‘Sexual selection.’ (Princeton University Press: Princeton, New Jersey)Beardsell C (1991) ‘Sites of faunal significance in the Western region of Melbourne (inland of the Princes Freeway).’ (Department of Conservation and Environment: Victoria)
Bennett, JH, Breed, WG, Hayman, DL, and Hope, RM (1989). Reproductive and genetic studies with a laboratory colony of the dasyurid marsupial Sminthopsis crassicaudata. Australian Journal of Zoology 37, 207–222.
| Reproductive and genetic studies with a laboratory colony of the dasyurid marsupial Sminthopsis crassicaudata.Crossref | GoogleScholarGoogle Scholar |
Candolin, U (2003). The use of multiple cues in mate choice. Biological Reviews 78, 575–595.
| The use of multiple cues in mate choice.Crossref | GoogleScholarGoogle Scholar |
Chargé, R, Teplitsky, C, Sorci, G, and Low, M (2014). Can sexual selection theory inform genetic management of captive populations? A review. Evolutionary Applications 7, 1120–1133.
| Can sexual selection theory inform genetic management of captive populations? A review.Crossref | GoogleScholarGoogle Scholar |
Charpentier, MJE, Boulet, M, and Drea, CM (2008). Smelling right: the scent of male lemurs advertises genetic quality and relatedness. Molecular Ecology 17, 3225–3233.
| Smelling right: the scent of male lemurs advertises genetic quality and relatedness.Crossref | GoogleScholarGoogle Scholar |
Cockburn, A (1989). Sex-ratio variation in marsupials. Australian Journal of Zoology 37, 467–479.
| Sex-ratio variation in marsupials.Crossref | GoogleScholarGoogle Scholar |
Cook, LE, Newton, AH, Hipsley, CA, and Pask, AJ (2021). Postnatal development in a marsupial model, the fat-tailed dunnart (Sminthopsis crassicaudata; Dasyuromorphia: Dasyuridae). Communications Biology 4, 1028.
| Postnatal development in a marsupial model, the fat-tailed dunnart (Sminthopsis crassicaudata; Dasyuromorphia: Dasyuridae).Crossref | GoogleScholarGoogle Scholar |
Darwin C (1859) ‘On the origin of species by means of natural selection.’ (Murray: London UK)
Department of Environment, Land, Water and Planning (DELWP) (2013) Advisory list of threatened vertebrate fauna in Victoria. Available at https://www.environment.vic.gov.au/__data/assets/pdf_file/0014/50450/Advisory-List-of-Threatened-Vertebrate-Fauna_FINAL-2013.pdf [Accessed 10 October 2016]
Drickamer, LC, Gowaty, PA, and Holmes, CM (2000). Free female mate choice in house mice affects reproductive success and offspring viability and performance. Animal Behaviour 59, 371–378.
| Free female mate choice in house mice affects reproductive success and offspring viability and performance.Crossref | GoogleScholarGoogle Scholar |
Ewer, RF (1968). A preliminary survey of the behaviour in captivity of the dasyurid marsupial, Sminthopsis crassicaudata (Gould). Zeitschrift für Tierpsychologie 25, 319–365.
| A preliminary survey of the behaviour in captivity of the dasyurid marsupial, Sminthopsis crassicaudata (Gould).Crossref | GoogleScholarGoogle Scholar |
Farquharson, KA, Hogg, CJ, and Grueber, CE (2017). Pedigree analysis reveals a generational decline in reproductive success of captive Tasmanian devil (Sarcophilus harrisii): implications for captive management of threatened species. Journal of Heredity 108, 488–495.
| Pedigree analysis reveals a generational decline in reproductive success of captive Tasmanian devil (Sarcophilus harrisii): implications for captive management of threatened species.Crossref | GoogleScholarGoogle Scholar |
Faust, LJ, and Thompson, SD (2000). Birth sex ratio in captive mammals: patterns, biases, and the implications for management and conservation. Zoo Biology 19, 11–25.
| Birth sex ratio in captive mammals: patterns, biases, and the implications for management and conservation.Crossref | GoogleScholarGoogle Scholar |
Fisher RA (1930) ‘The genetical theory of natural selection.’ (Clarendon Press: Oxford)
Flora and Fauna Guarantee - Scientific Advisory Committee (FFG-SAC) (2022) Preliminary recommendation on a nomination for listing Sminthopsis crassicaudata, fat-tailed dunnart. Department of Natural Resources and Environment, Melbourne.
Friard, O, and Gamba, M (2016). BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods in Ecology and Evolution 7, 1325–1330.
| BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations.Crossref | GoogleScholarGoogle Scholar |
Godfrey, GK (1969). The influence of increased photoperiod on reproduction in the dasyurid marsupial, Sminthopsis crassicaudata. Journal of Mammalogy 50, 132–133.
| The influence of increased photoperiod on reproduction in the dasyurid marsupial, Sminthopsis crassicaudata.Crossref | GoogleScholarGoogle Scholar |
Godfrey, GK, and Crowcroft, P (1971). Breeding the fat-tailed marsupial mouse in captivity. International Zoo Yearbook 11, 33–38.
| Breeding the fat-tailed marsupial mouse in captivity.Crossref | GoogleScholarGoogle Scholar |
Hartnett, CM, Parrott, ML, Mulder, RA, Coulson, G, and Magrath, MJL (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 |
Homan, P (2022). Surveys of vertebrate fauna on the northern outskirts of metropolitan Melbourne, 2006–2022: (1) mammals. Victorian Naturalist 139, 173–183.
Hope, PJ, Pyle, D, Daniels, CB, Chapman, I, Horowitz, M, Morley, JE, Trayhurn, P, Kumaratilake, J, and Wittert, G (1997). Identification of brown fat and mechanisms for energy balance in the marsupial, Sminthopsis crassicaudata. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 273, R161–R167.
| Identification of brown fat and mechanisms for energy balance in the marsupial, Sminthopsis crassicaudata.Crossref | GoogleScholarGoogle Scholar |
IUCN (2022) The IUCN red list of threatened species (version 2022-1). Available at http:9//www.iucnredlist.org. [Accessed 23 July 2022]
Jennions, MD, and Petrie, M (2000). Why do females mate multiply? A review of the genetic benefits. Biological Reviews of the Cambridge Philosophical Society 75, 21–64.
| Why do females mate multiply? A review of the genetic benefits.Crossref | GoogleScholarGoogle Scholar |
Johansson, BG, and Jones, TM (2007). The role of chemical communication in mate choice. Biological Reviews 82, 265–289.
| The role of chemical communication in mate choice.Crossref | GoogleScholarGoogle Scholar |
Landry, C, Garant, D, Duchesne, P, and Bernatchez, L (2001). ‘Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proceedings of the Royal Society of London B: Biological Sciences 268, 1279–1285.
| ‘Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar).Crossref | GoogleScholarGoogle Scholar |
Martin, MS, and Shepherdson, DJ (2012). Role of familiarity and preference in reproductive success in ex situ breeding programs. Conservation Biology 26, 649–656.
| Role of familiarity and preference in reproductive success in ex situ breeding programs.Crossref | GoogleScholarGoogle Scholar |
Mays, HL, and Hill, GE (2004). Choosing mates: good genes versus genes that are a good fit. Trends in Ecology & Evolution 19, 554–559.
| Choosing mates: good genes versus genes that are a good fit.Crossref | GoogleScholarGoogle Scholar |
Møller, AP (1988). Female choice selects for male sexual tail ornaments in the monogamous swallow. Nature 332, 640–642.
| Female choice selects for male sexual tail ornaments in the monogamous swallow.Crossref | GoogleScholarGoogle Scholar |
Morton, SR (1978a). An ecological study of Sminthopsis crassicaudata (Marsupialia: Dasyuridae) III. Reproduction and life history. Wildlife Research 5, 183–211.
| An ecological study of Sminthopsis crassicaudata (Marsupialia: Dasyuridae) III. Reproduction and life history.Crossref | GoogleScholarGoogle Scholar |
Morton, SR (1978b). An ecological study of Sminthopsis crassicaudata (Marsupialia: Dasyuridae) II. Behaviour and social organization. Wildlife Research 5, 163–182.
| An ecological study of Sminthopsis crassicaudata (Marsupialia: Dasyuridae) II. Behaviour and social organization.Crossref | GoogleScholarGoogle Scholar |
Murphy H, van Leeuwen S (2021) Australia state of the environment 2021. Biodiversity, independent report to the Australian Government Minister for the Environment, Commonwealth of Australia, Canberra. https://doi.org/10.26194/ren9-3639
Panhuis, TM, Butlin, R, Zuk, M, and Tregenza, T (2001). Sexual selection and speciation. Trends in Ecology & Evolution 16, 364–371.
| Sexual selection and speciation.Crossref | GoogleScholarGoogle Scholar |
Parrott, ML, Ward, SJ, and Temple-Smith, PD (2007). Olfactory cues, genetic relatedness and female mate choice in the agile antechinus (Antechinus agilis). Behavioral Ecology and Sociobiology 61, 1075–1079.
| Olfactory cues, genetic relatedness and female mate choice in the agile antechinus (Antechinus agilis).Crossref | GoogleScholarGoogle Scholar |
Parrott, ML, Ward, SJ, Temple-Smith, PD, and Selwood, L (2015). Females choose mates based on genetic relatedness in a small dasyurid marsupial, the agile antechinus (Antechinus agilis). PLoS ONE 10, e0122381.
| Females choose mates based on genetic relatedness in a small dasyurid marsupial, the agile antechinus (Antechinus agilis).Crossref | GoogleScholarGoogle Scholar |
Parrott, ML, Coetsee, AL, Hartnett, CM, and Magrath, MJL (2017). New hope for the eastern barred bandicoot Perameles gunnii after 27 years of recovery effort. International Zoo Yearbook 51, 154–164.
| New hope for the eastern barred bandicoot Perameles gunnii after 27 years of recovery effort.Crossref | GoogleScholarGoogle Scholar |
Parrott, ML, Nation, A, and Selwood, L (2019). Female mate choice significantly increases captive breeding success, and scents can be frozen to determine choice, in the stripe-faced dunnart. Applied Animal Behaviour Science 214, 95–101.
| Female mate choice significantly increases captive breeding success, and scents can be frozen to determine choice, in the stripe-faced dunnart.Crossref | GoogleScholarGoogle Scholar |
Penn, DJ, and Potts, WK (1999). The evolution of mating preferences and major histocompatibility complex genes. The American Naturalist 153, 145–164.
| The evolution of mating preferences and major histocompatibility complex genes.Crossref | GoogleScholarGoogle Scholar |
Poiley, SM (1960). A systematic method of breeder rotation for non-inbred laboratory colonies. Proceedings Animal Care Panel 10, 159–166.
Reby, D, Hewison, M, Izquierdo, M, and Pépin, D (2001). Red deer (Cervus elaphus) hinds discriminate between the roars of their current harem-holder stag and those of neighbouring stags. Ethology 107, 951–959.
| Red deer (Cervus elaphus) hinds discriminate between the roars of their current harem-holder stag and those of neighbouring stags.Crossref | GoogleScholarGoogle Scholar |
Rich, TJ, and Hurst, JL (1998). Scent marks as reliable signals of the competitive ability of mates. Animal Behaviour 56, 727–735.
| Scent marks as reliable signals of the competitive ability of mates.Crossref | GoogleScholarGoogle Scholar |
Robert, KA, and Schwanz, LE (2011). Emerging sex allocation research in mammals: marsupials and the pouch advantage. Mammal Review 41, 1–22.
| Emerging sex allocation research in mammals: marsupials and the pouch advantage.Crossref | GoogleScholarGoogle Scholar |
Roberts, SC, and Gosling, LM (2003). Genetic similarity and quality interact in mate choice decisions by female mice. Nature Genetics 35, 103–106.
| Genetic similarity and quality interact in mate choice decisions by female mice.Crossref | GoogleScholarGoogle Scholar |
RStudio Team (2018) RStudio: integrated development for R. (RStudio, Inc.: Boston, MA) Available at http://www.rstudio.com/
Russell, EM (1982). Parental investment and desertion of young in marsupials. The American Naturalist 119, 744–748.
| Parental investment and desertion of young in marsupials.Crossref | GoogleScholarGoogle Scholar |
Sato, A, Ozawa, N, and Karino, K (2014). Variation in female guppy preference for male olfactory and visual traits. Journal of Ethology 32, 137–143.
| Variation in female guppy preference for male olfactory and visual traits.Crossref | GoogleScholarGoogle Scholar |
Schulte-Hostedde, AI, Zinner, B, Millar, JS, and Hickling, GJ (2005). Restitution of mass–size residuals: validating body condition indices. Ecology 86, 155–163.
| Restitution of mass–size residuals: validating body condition indices.Crossref | GoogleScholarGoogle Scholar |
Scicluna, EL, Gill, BP, Robert, KA, and Cooper, S (2021). Fat-tailed dunnarts (Sminthopsis crassicaudata) of the Werribee grasslands: a case study of a species in decline. Australian Journal of Zoology 69, 27–32.
| Fat-tailed dunnarts (Sminthopsis crassicaudata) of the Werribee grasslands: a case study of a species in decline.Crossref | GoogleScholarGoogle Scholar |
Smith, MJ, Bennett, JH, and Chesson, CM (1978). Photoperiod and some other factors affecting reproduction in female Sminthopsis crassicaudata (Gould) (Marsupialia: Dasyuridae) in captivity. Australian Journal of Zoology 26, 449–463.
| Photoperiod and some other factors affecting reproduction in female Sminthopsis crassicaudata (Gould) (Marsupialia: Dasyuridae) in captivity.Crossref | GoogleScholarGoogle Scholar |
Steele, WK, and Brunner, H (2021). Contents of eastern barn owl ‘Tyto delicatula’ regurgitation pellets at the Werribee Sewege Farm, Victoria, suggest possible decline in abundance of fat-tailed dunnart ‘Sminthopsis crassicaudata’. The Victorian Naturalist 138, 171–175.
Trivers, RL, and Willard, DE (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 90–92.
| Natural selection of parental ability to vary the sex ratio of offspring.Crossref | GoogleScholarGoogle Scholar |
Tyndale-Biscoe CH, Renfree M (1987) Breeding biology of marsupials by family. In ‘Reproductive Physiology of Marsupials’. pp. 16. (Cambridge University Press: New York)
Victorian Government (2023) Victorian Government Gazette No. G 8. Victorian Government Printer, Victoria.
Voigt, CC, Behr, O, Caspers, B, von Helversen, O, Knörnschild, M, Mayer, F, and Nagy, M (2008). Songs, scents, and senses: sexual selection in the greater sac-winged bat, Saccopteryx bilineata. Journal of Mammalogy 89, 1401–1410.
| Songs, scents, and senses: sexual selection in the greater sac-winged bat, Saccopteryx bilineata.Crossref | GoogleScholarGoogle Scholar |
Wedekind, C (2002). Manipulating sex ratios for conservation: short-term risks and long-term benefits. Animal Conservation 5, 13–20.
| Manipulating sex ratios for conservation: short-term risks and long-term benefits.Crossref | GoogleScholarGoogle Scholar |
