Opportunity for female mate choice improves reproductive outcomes in the conservation breeding program of the eastern barred bandicoot (Perameles gunnii)

Highlights

• In mate choice trials, most females interacted more with one male over the other.

• Female mate choice led to increased reproductive success in this endangered bandicoot.

• Pairing with preferred males reduced the time to conception of pouch young.

Abstract

Captive breeding is fundamental to recovery programs for many endangered species. Most programs seek to maximise retention of genetic variation and minimise inbreeding risk by assigning individuals to pre-determined pairings, but the reproductive outcomes of such pairings are often poor. There is evidence that pairing individuals in captivity that are instead genetically and behaviourally compatible can result in improved reproductive success, and that the resulting offspring perform better when released into the wild. Evidence is also 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 resulted 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.

Introduction

Sexual selection theory predicts that females should be the more selective sex in choosing mates due to differential investment in gamete production and parental care (Trivers, 1972). For males, reproductive success tends to increase with the number of mates acquired (Bateman, 1948), but females are often limited in their reproductive opportunities, so should invest more selectively in reproduction (Andersson, 1994, Kokko et al., 2003). Where females can choose between numerous males, they will commonly increase their fitness, and that of their offspring, by selecting genetically compatible mates, or mates with ‘good genes’ that offspring may inherit (Ahtiainen et al., 2004, Tregenza and Wedell, 2000).

Mate choice may help maintain genetic diversity at both the individual and population levels. ‘Heterozygosity theory’ (Brown, 1997, Brown, 1999, Kempenaers, 2007) predicts directional female preference for males with greater allelic variety, and avoidance of inbreeding by preference for non-related males (Brown, 1997, Trivers, 1972, Weatherhead et al., 1999). Heterozygosity, mate preference, and subsequent reproductive success are united in studies across diverse taxa (Hoffman et al., 2007, Ilmonen et al., 2009, Marshall et al., 2003).

While genetic diversity is an important factor, combinations of genes, arising from the interactions of parental genes and linked to physiological and behavioural attributes, may be more beneficial than heterozygosity alone (Neff and Pritcher, 2005, Puurtinen et al., 2009). The prediction is that females will choose mates that produce offspring with optimum genetic variety and gene combinations (Colegrave et al., 2002; Neff and Pitcher, 2005).

Evaluation of potential mates generally involves multiple cues, with foundations in morphology, physiology and behaviour (Jennions and Petrie, 1997). In mammalian reproduction, olfaction is likely the prime sensory modality (Roberts and Gosling, 2004), and the reliability of olfactory cues as indicators of male quality has been explored in some detail (Charpentier et al., 2008, Johansson and Jones, 2007). Females reportedly use scent to assess kinship (Parrott et al., 2007), social dominance (Drickamer et al., 2000), and genetic heterozygosity at key gene loci (Hoffman et al., 2007, Ilmonen et al., 2009), including at the Major Histocompatibility Complex which is active in immunity (Huchard et al., 2010, Huchard et al., 2013).

Mate choice is thus an important element of reproduction in many taxa (Davies et al., 2012, Kappeler, 2010). However, mate selection in the wild typically contrasts with captive breeding, where individuals are assigned a mate, usually with the aim of minimising relatedness of paired individuals to retain maximum genetic diversity in the captive population (Ballou and Lacy, 1995, Earnhardt et al., 2001). This is an important objective, but provides no guarantee of genetic and/or behavioural compatibility between individuals, potentially constraining the productivity of captive breeding programs (Asa et al., 2011, Møller and Legendre, 2001, Wolf et al., 2000).

Captive-bred animals can also lack some physiological and behavioural attributes of their wild conspecifics, attributed to either inbreeding (Hedrick and Kalinowski, 2000, Robert, 2009) or adaptation to captivity (Araki et al., 2007, Frankham, 2008, Lynch and O’Hely, 2001). Both have negative implications for the fitness of released animals, as highlighted in some extensive reviews of reintroduction/relocation survival rates (Fischer and Lindenmayer, 2000, Jule et al., 2008). In the feathertail glider (Acrobates pygmaeus), for example, the poor expression of torpor and thermal performance seen in captive-bred animals may seriously impact their survival in the wild (Geiser and Ferguson, 2001).

Mate choice may enhance genetic and behavioural compatibility between mates, and thus improve both the reproductive success within captive breeding programs (Asa et al., 2011, Grahn et al., 1998), and fitness of released offspring, with such outcomes reported in insects (Anderson et al., 2007), birds (Bluhm and Gowaty, 2004, Ihle et al., 2015), and mammals (Drickamer et al., 2000). In one of only very few mate choice studies in marsupial species, female agile antechinus (Antechinus agilis) chose to mate with males least related to themselves based on olfactory cues, thus avoiding possibly deleterious effects of inbreeding (Parrott et al., 2007). Pairing of behaviourally compatible animals in captivity has led to better reproductive performance (Spoon et al., 2006), reduced aggression between mates (Gold and Maple, 1994, Powell, 2010, Powell and Gartner, 2011), and, in species that provide bi-parental care, greater success in raising young when compared to random pairings (Ihle et al., 2015).

In this study, we investigated the potential benefits of mate choice within conservation breeding of the critically endangered mainland eastern barred bandicoot, Perameles gunnii (EBB). Once abundant on the basalt plains of south-western Victoria and south-eastern South Australia, this species is now extinct in the wild on mainland Australia (Department of Environment Land Water Planning, 2013). There are an estimated 1200 individuals, including reintroduced and captive populations, descended from only 19–23 founders taken into captivity from the last known wild population in the early 1990s (Coetsee, 2016). Reintroduced populations have since lost significant genetic diversity of 25–35% (Weeks et al., 2013). Twenty-seven years of captive breeding has produced nearly 900 offspring (Coetsee, 2016), but breeding records indicate that only about half of the assigned pairings produced offspring within three months of pairing (n = 180 pairs; Hartnett, 2015). This compares unfavourably to the mean percentage of 88% of free-ranging females found to be breeding each year over a four-year period (n = 294 females; Coetsee – unpubl. data, Woodlands Historic Park).

We conducted an experimental study in which female bandicoots were given the opportunity to interact with two different males over an extended period of time. We (i) assessed female preference for particular males, and (ii) determined if measures of reproductive success were greater for females paired with preferred versus non-preferred males. These findings should determine whether the incorporation of mate choice could benefit the breeding program of this species, but also contribute to understanding the value of mate choice in conservation-based captive breeding more generally.