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Opportunity for Female Mate Choice Improves Reproductive Outcomes in the Conservation Breeding Program of the Eastern Barred

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Opportunity for Female Mate Choice Improves Reproductive Outcomes in the Conservation Breeding Program of the Eastern Barred Applied Animal Behaviour Science 199 (2018) 67–74 Contents lists available at ScienceDirect Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim Research Paper Opportunity for female mate choice improves reproductive outcomes in the T conservation breeding program of the eastern barred bandicoot (Perameles gunnii) ⁎ Christine M. Hartnetta,b, , Marissa L. Parrottb, Raoul A. Muldera, Graeme Coulsona, Michael J.L. Magrathb a School of Biosciences, The University of Melbourne, Victoria 3010, Australia b Department of Wildlife Conservation and Science, Zoos Victoria, Parkville, Victoria 3052, Australia ARTICLE INFO ABSTRACT Keywords: Captive breeding is fundamental to recovery programs for many endangered species. Most programs seek to Mate choice maximise retention of genetic variation and minimise inbreeding risk by assigning individuals to pre-determined Mate preference pairings, but the reproductive outcomes of such pairings are often poor. There is evidence that pairing in- Olfactory communication dividuals in captivity that are instead genetically and behaviourally compatible can result in improved re- Genetic compatibility productive success, and that the resulting offspring perform better when released into the wild. Evidence is also Behavioural compatibility mounting that such compatible outcomes can be achieved by allowing female mate choice. We investigated whether the reproductive success of captive endangered eastern barred bandicoots (Perameles gunnii) improved when females were permitted to choose their mate. Over a 21 day period, we allowed females to simultaneously evaluate two males that were unrelated to the female via interaction through perforated clear acrylic barriers, which permitted visual, auditory and olfactory, but not physical, contact. We determined female preferences by measuring how much time they spent interacting with each male, and whether they showed behavioural signs of receptivity. We then paired females with either their preferred or non-preferred male, and recorded the time to conception and number of pouch young produced. Based on the interaction choice trials, females paired with preferred males were significantly more likely to produce young (p = 0.03). These preferred pairings also re- sulted in earlier conception of young than non-preferred pairings (p = 0.008). These findings could improve productivity of the eastern barred bandicoot breeding program and, more generally, support the incorporation of mate choice into conservation breeding programs for other species wherever practical. 1. Introduction 1999; Kempenaers, 2007) predicts directional female preference for males with greater allelic variety, and avoidance of inbreeding by Sexual selection theory predicts that females should be the more preference for non-related males (Brown, 1997; Trivers, 1972; selective sex in choosing mates due to differential investment in gamete Weatherhead et al., 1999). Heterozygosity, mate preference, and sub- production and parental care (Trivers, 1972). For males, reproductive sequent reproductive success are united in studies across diverse taxa success tends to increase with the number of mates acquired (Bateman, (Hoffman et al., 2007; Ilmonen et al., 2009; Marshall et al., 2003). 1948), but females are often limited in their reproductive opportunities, While genetic diversity is an important factor, combinations of genes, so should invest more selectively in reproduction (Andersson, 1994; arising from the interactions of parental genes and linked to physiolo- Kokko et al., 2003). Where females can choose between numerous gical and behavioural attributes, may be more beneficial than hetero- males, they will commonly increase their fitness, and that of their off- zygosity alone (Neff and Pritcher, 2005; Puurtinen et al., 2009). The spring, by selecting genetically compatible mates, or mates with ‘good prediction is that females will choose mates that produce offspring with genes’ that offspring may inherit (Ahtiainen et al., 2004; Tregenza and optimum genetic variety and gene combinations (Colegrave et al., Wedell, 2000). 2002;Neff and Pitcher, 2005). Mate choice may help maintain genetic diversity at both the in- Evaluation of potential mates generally involves multiple cues, with dividual and population levels. ‘Heterozygosity theory’ (Brown, 1997, foundations in morphology, physiology and behaviour (Jennions and ⁎ Corresponding author at: Department of Wildlife Conservation and Science, Zoos Victoria, Parkville, Victoria, 3052, Australia. E-mail addresses: [email protected], [email protected] (C.M. Hartnett). http://dx.doi.org/10.1016/j.applanim.2017.10.008 Received 14 December 2016; Received in revised form 4 September 2017; Accepted 12 October 2017 Available online 20 October 2017 0168-1591/ © 2017 Elsevier B.V. All rights reserved. C.M. Hartnett et al. Applied Animal Behaviour Science 199 (2018) 67–74 Petrie, 1997). In mammalian reproduction, olfaction is likely the prime particular males, and (ii) determined if measures of reproductive suc- sensory modality (Roberts and Gosling, 2004), and the reliability of cess were greater for females paired with preferred versus non-pre- olfactory cues as indicators of male quality has been explored in some ferred males. These findings should determine whether the incorpora- detail (Charpentier et al., 2008; Johansson and Jones, 2007). Females tion of mate choice could benefit the breeding program of this species, reportedly use scent to assess kinship (Parrott et al., 2007), social but also contribute to understanding the value of mate choice in con- dominance (Drickamer et al., 2000), and genetic heterozygosity at key servation-based captive breeding more generally. gene loci (Hoffman et al., 2007; Ilmonen et al., 2009), including at the Major Histocompatibility Complex which is active in immunity 2. Methods (Huchard et al., 2010, 2013). Mate choice is thus an important element of reproduction in many 2.1. Study animals and maintenance taxa (Davies et al., 2012; Kappeler, 2010). However, mate selection in the wild typically contrasts with captive breeding, where individuals This study received approval from the Zoos Victoria Animal Ethics are assigned a mate, usually with the aim of minimising relatedness of Committee (ZV14006), in accordance with the Australian Code of paired individuals to retain maximum genetic diversity in the captive Practice for the Care and Use of Animals for Scientific Purposes. Captive population (Ballou and Lacy, 1995; Earnhardt et al., 2001). This is an eastern barred bandicoots were studied at Werribee Open Range Zoo important objective, but provides no guarantee of genetic and/or be- (WORZ), Victoria, Australia. The breeding facility at this site can house havioural compatibility between individuals, potentially constraining up to 36 bandicoots, and contributes to the captive insurance and re- the productivity of captive breeding programs (Asa et al., 2011; Møller lease program for this species. and Legendre, 2001; Wolf et al., 2000). We performed 22 mate choice trials over two years (2014–2015), Captive-bred animals can also lack some physiological and beha- with a total of 18 females (four being used twice in trials) and 20 males vioural attributes of their wild conspecifics, attributed to either in- (ten being used in 2–4 trials) observed across the two years. The use of breeding (Hedrick and Kalinowski, 2000; Robert, 2009) or adaptation some animals in more than one trial was necessitated by the limited to captivity (Araki et al., 2007; Frankham, 2008; Lynch and O’Hely, availability of animals, and was based on whether animals had already 2001). Both have negative implications for the fitness of released ani- been designated for pairing in a previous trial. Two females used in mals, as highlighted in some extensive reviews of reintroduction/re- preference trials were not paired but were released to the wild as part of location survival rates (Fischer and Lindenmayer, 2000; Jule et al., a reintroduction program. Trials ran from early September to late 2008). In the feathertail glider (Acrobates pygmaeus), for example, the October in 2014, and from early June to mid-October in 2015, falling poor expression of torpor and thermal performance seen in captive-bred within the peak breeding season (winter-spring) for the eastern barred animals may seriously impact their survival in the wild (Geiser and bandicoot (Winnard, 2010). Although breeding in this species can be Ferguson, 2001). temperature-dependent, it has been observed year-round where con- Mate choice may enhance genetic and behavioural compatibility ditions are favourable (Winnard, 2010). Like all Peramelid species, fe- between mates, and thus improve both the reproductive success within male EBBs are polyoestrous, and may produce up to five litters per year captive breeding programs (Asa et al., 2011; Grahn et al., 1998), and (Heinsohn, 1966), suggesting receptivity throughout the year. fitness of released offspring, with such outcomes reported in insects In 2014, all study animals were sourced from the existing captive (Anderson et al., 2007), birds (Bluhm and Gowaty, 2004, Ihle et al., population. In 2015, ten new animals (five of each sex) were sourced 2015), and mammals (Drickamer et al., 2000). In one of only very few from a wild population at the Mt. Rothwell Biodiversity Interpretation mate choice studies in marsupial species, female agile antechinus Centre. All animals were housed individually in purpose-built bandi- (Antechinus agilis)
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