MHC diversity and female age underpin reproductive success in an Australian icon; the Tasmanian Devil

Abstract

Devil Facial Tumour Disease (DFTD), a highly contagious cancer, has decimated Tasmanian devil (Sarcophilus harrisii) numbers in the wild. To ensure its long-term survival, a captive breeding program was implemented but has not been as successful as envisaged at its launch in 2005. We therefore investigated the reproductive success of 65 captive devil pair combinations, of which 35 produced offspring (successful pairs) whereas the remaining 30 pairs, despite being observed mating, produced no offspring (unsuccessful pairs). The devils were screened at six MHC Class I-linked microsatellite loci. Our analyses revealed that younger females had a higher probability of being successful than older females. In the successful pairs we also observed a higher difference in total number of heterozygous loci, i.e. when one devil had a high total number of heterozygous loci, its partner had low numbers. Our results therefore suggest that devil reproductive success is subject to disruptive MHC selection, which to our knowledge has never been recorded in any vertebrate. In order to enhance the success of the captive breeding program the results from the present study show the importance of using young (2-year old) females as well as subjecting the devils to MHC genotyping.

Figure 1

Relationship between female age and the success of reproduction in Tasmanian devil pairs (a). Points with error bars depict reproductive success (±95% CI) of pairs across female age. Grey line shows the binomial model prediction of this relationship with the 95% confidence interval (grey polygon).

Figure 2

(a) Mode prediction of the interaction between the number of male and female heterozygous loci. The color scale (within the data range) and contour lines (across the entire range of female and male heterozygous loci) indicate the probability of being successful according to the combination of the number of male and female heterozygous loci. (b) Diagonal section of the model prediction shown in (a) across the optimal pair combinations with 95% confidence interval.