Adaptation to captivity and management practices
For MHC genes, rare allele and heterozygous advantage are two types of balancing selection that have been suggested to be important in maintaining high levels of adaptive genetic diversity (Sommer, 2005). Assuming that rare and divergent MHC genotypes are more likely to induce host control on gut microbes, giving a fitness advantage to the host, the co-evolutionary arm race with gut microbes will foster adaptation from microorganisms to not be targeted by common MHC alleles (Kubinak et al., 2012). However, the evolutionary time lag of these antagonistic responses can lead to variation in fitness in a cyclic manner and microbe-driven selection could vary over time and space and between E-mink populations. This mechanism could be of influence in the western E-mink population, given that the breeding program started in 2013 and individuals from the wild are still being captured to increase founder size in the program from the natural habitat. Moreover, low MHC class II gene diversity in the eastern population might indicate that non-evolutionary forces overshadow balancing selection for this locus, which could be mainly explained by extensive constrains in the mating system for a long period of time.
Inadvertent genetic adaptation to captivity for endangered species has been documented over recent years (reviewed in Frankham, 2008). This has been related to a fitness reduction when animals are released in the wild environment, increasing with the numbers of captive-bred generations, including changes in reproductive success, morphology and behavior (Williams & Hoffman, 2009; Willoughby & Christie, 2019). Becker et al. (2009) previously investigated the MHC-II DRB gene in the captive eastern E-mink population, and detected nine alleles, representing 6 motifs. However, ten years later, we observed 3 motifs in the eastern group. The EEP in Estonia started in 1992 and has not been supplemented by wild individuals for at least 25 generations (T. Maran, pers. comm., 2021). Moreover, given the moderate success of the breeding program due to captive-born male behavior (Kiik et al., 2013), this suggests that high number of generations in captivity led to loss of genetic diversity and deleterious genetic fixation took place for this population (Woodworth et al., 2002; Frankham, 2008; Witzenberger & Hochkirch, 2011; Parmar et al., 2017). Even though 90% of the initial gene diversity has been maintained through studbook calculations (T. Maran, pers. comm., 2021), it is likely that studbook measurements might not reflect this trend for all E-mink genes. However, different management strategies have been proposed to mitigate fitness reduction for future reintroduction (reviewed in Williams & Hoffman, 2009) that could be implemented for the E-mink.
One strategy is to limit the number of generations captivity through the use of artificial insemination (AI) and gametes cryopreservation. AI allows to balance the genetic contribution between males, even with individuals showing abnormal breeding behavior. Gametes cryopreservation could extend the generation intervals, only requiring mature females kept in captivity. These tools have been conducted in the CBP of the black footed ferret (Mustela nigripes ) and benefited the program, notably by using sperm that were stored as long as 20 years (Howard et al., 2015). However, these technics present serious limitations as they are expensive to put in place, demand expertise and investigation for success in every single species, and it is therefore unlikely that they become tools on a regular basis for the E-mink programs at this time.
Another strategy is to translocate animals between breeding centers for reproduction to prevent loss of genetic diversity. Similar to the western captive population of E-mink, these translocations could be composed of wild-born individuals, free of captive selection pressure (Schulte-Hostedde & Mastromonaco, 2015). Occasional translocations from western to eastern captive populations could also be conducted and would potentially mitigate the modest reproductive success within the program. It is worth noting that wild-born animals have been out of reach from the EEP breeding stock so far. However, conducting preliminary MHC variation assessment on reintroduced animals from the eastern stock present in Hiiumaa island, as they no longer face captivity for a number of generations, could be used to identify potential assets to the current breeding stock.
Captivity has been shown to alter gut microbial communities (McKenzie et al., 2017). Combined with this traditional conservation efforts, microbial rescue could also help improve success of managing at-risk populations. For example, the most common cause of mortality in captive cheetahs (Acinonyx jubatus ) is bacterial infection, possibly because of an increase in pathogenic taxa compared to wild conspecifics (Wasimuddin et al., 2017). Microbial rescue, using probiotics, can stabilize the composition of the gut microbiota of dolphin in captivity (Lagenorhynchus obliquidens , Cardona et al., 2018). Implementing wild-like diet-based enrichment could also mitigate captivity effects on gut microbial communities in the same way as captive selection (Mueller et al., 2019; Trevelline et al., 2019; van Leeuwen et al., 2020).
These types of strategies could increase adaptive genetic diversity related to immunomodulation and therefore a fitness advantage to the mink once reintroduced. Coupled with a more in-depth investigation on the gut microbiota of the E-mink according to diet and environment manipulation, these technics can have synergetic effects and foster the success of the CBPs (Gould et al., 2018; West et al., 2019). This first look into the connection between management strategies, genetic diversity and gut bacteria within the CBPs of the E-mink allowed preliminary assessment of the current situation. It also offers many axes of further research and potential strategies with the on-going challenges that many ex situ conservation programs face to mitigate species extinction.