0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
Incestuous pairs (18 broods) Non-incestuous pairs (26 broods)
*
n.s.
n.s.
Discussion
Extra-group mating for inbreeding avoidance
Inbreeding has been shown to reduce reproductive performance in many animal species (Amos et al. 2001, Charlesworth & Charlesworth 1987, Keller
& Waller 2002, Kempenaers 2007), indicating selection against breeding with relatives (Pusey & Wolf 1996). In M. coronatus, restricted dispersal and limited breeding positions limit optimal social mate choice, and some individuals engage in incestuous pairings. Although such pairs often divorce after some time (Hall ML, Kingma SA, Peters A, unpublished data), many do initially nest together. We tested here whether females in incestuous pairs can avoid inbreeding through copulations with genetically dissimilar males outside the cooperative group.
Inbreeding avoidance through EP mating with genetically dissimilar males has recently become one popular hypothesis to explain multiple mating by females (Akçay & Roughgarden 2007, Kempenaers 2007, Mays et al.
2008). In line with this hypothesis, we found that M. coronatus females that were paired to a first-order relative were nearly 15 times more likely to produce EG offspring than females with a less related social male (Fig. 3.2).
Those EG males were less related to the female than her social male was (Fig. 3.3), and therefore it is likely that the resulting offspring are more heterozygous than they would have been if fertilised by the social male.
Offspring are predicted to benefit from increased heterozygosity because recessive deleterious alleles are less likely to be expressed than in more homozygous inbred offspring (Keller & Waller 2002, Lynch et al. 1995).
Although we did not have the data to show that hatchability of eggs was associated with heterozygosity, we do show that hatching success of M.
coronatus eggs decreases by more than 20% with increasing genetic similarity of the social pair. Especially considering that we could not correct for parentage in our conservative analysis and rates of hatching failure in incestuous pairs are probably even higher, this implies that inbreeding exerts a substantial cost on parental fitness. Thus, EG mating is one way in which females can avoid the negative effects of inbreeding.
Synchronisation to overcome constraints on EG mating
Overall rates of EGP are much lower in M. coronatus than in its congeners (6% vs. 40 to 80% of offspring; see Kingma et al. 2009; chapter 2), probably as a result of ecological constraints that reduce the availability of potential EG partners (Kingma et al. 2009). Here, we show that the number of nearby males had a positive effect on the incidence of EGP (Fig. 3.4), confirming this reasoning. Additionally, M. coronatus males are poorly adapted to EP mating, with small testes and cloacal protuberances (Kingma et al. 2009; see Fig. 2.1).
Breeding is irregular and can take place at any time of the year, and if male fertility tracks the fertile period of his social partner, this implies that availability of fertile males is even further reduced in M. coronatus. Reduced periods of fertility of males can be expected as the size of cloacal protuberances (an indicator of sperm production) has been shown to peak around egg laying of their partner in other species with low EPP (e.g., in bearded tits Panurus biarmicus; Sax & Hoi 1998). Altogether, the fact that females can be constrained in pursuing EP copulations raises the question
how they nonetheless can achieve this when they greatly benefit from EG mating (i.e., to avoid inbreeding).
We found several indications that female M. coronatus in incestuous pairs adopt active strategies to overcome the constraints of EG mating. First, incestuous pairs laid eggs when they were nearly twice as likely as non-incestuous pairs to have neighbors that were also around egg-laying (Fig.
3.6), suggesting that females synchronise breeding with fertility of neighboring males. Second, females with related social males that mated EG laid their eggs more synchronously with - and consistently shortly after - the female of the EG sire than females that had EGP for other (unidentified) reasons (Fig. 3.5a). Third, EG offspring of females with related males were (nearly always) sired by neighboring males, whereas EG offspring of females with an unrelated partner were sired by males from further away (Fig. 3.5b).
Female song rates are reduced during the pre-laying period, and males invest heavily in mate-guarding by maintaining close proximity to their partner until she lays her first egg (Hall & Peters 2009). M. coronatus females seeking EP copulations could therefore potentially use reduced female song rates as a cue to the specific period of fertility of neighbors, and target neighboring males when they are unconstrained by mate-guarding. This suggests that females in incestuous pairs actively ensure the presence of fertile EG males to facilitate EG copulations. This result forms, to our knowledge, the first empirical indication that EP mating to avoid inbreeding can be achieved by females through adopting an active pre-copulatory behavioural strategy.
Our results may have broad implications for the understanding of the evolution of promiscuity. The fact that female strategies may affect the correlation between ecological factors and the incidence of EPP should be taken into account when considering the relationship between those.
Additionally, we suggest that EP mating for inbreeding avoidance may be a more active strategy than often assumed, particularly in view of the lack of evidence for post-copulatory sperm selection (Denk et al. 2005). Therefore, our results form a considerable contribution to the discussion whether EP mating and inbreeding avoidance derive through active or primarily passive mechanism (i.e., sperm competition).
Acknowledgements
We are extremely grateful to E. Fricke and G. Segelbacher for help with the molecular work, to the staff at the Mornington Wildlife Sanctuary and the Australian Wildlife Conservancy for logistical support, and to our team of field assistants for their hard work in the field. All fieldwork was performed with permission from the Max Planck Institute for Ornithology Animal Ethics Committee, the Australian Wildlife Conservancy, the Western Australia Department of Conservation and Land Management (Licences BB002178 and BB002311), and the Australian Bird and Bat Banding Scheme (Authority 2230 and 2073). The research was funded by the “Minerva Sonderprogramm zur Förderung hervorragender Wissenschaftlerinnen” of the Max Planck Society (to AP).