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.