Population correlates of rapid captive‐induced maladaptation in a wild fish

Abstract

Understanding the extent to which captivity generates maladaptation in wild species can inform species recovery programs and elucidate wild population responses to novel environmental change. Although rarely quantified, effective population size (Ne) and genetic diversity should influence the magnitude of plastic and genetic changes manifested in captivity that reduce wild fitness. Sexually dimorphic traits might also mediate consequences of captivity. To evaluate these relationships, we generated >600 full‐ and half‐sibling families from nine wild brook trout populations, reared them for one generation under common, captive environmental conditions and contrasted several fitness‐related traits in wild versus captive lines. We found substantial variation in lifetime success (lifetime survival and reproductive success) and life history traits among wild populations after just one captive generation (fourteen‐ and threefold ranges across populations, respectively). Populations with lower heterozygosity showed lower captive lifetime success, suggesting that captivity generates maladaptation within one generation. Greater male‐biased mortality in captivity occurred in populations having disproportionately higher growth rates in males than females. Wild population Ne and allelic diversity had little or no influence on captive trait expression and lifetime success. Our results have four conservation implications: (i) Trait values and lifetime success were highly variable across populations following one generation of captivity. (ii) Maladaptation induced by captive breeding might be particularly intense for the very populations practitioners are most interested in conserving, such as those with low heterozygosity. (iii) Maladaptive sex differences in captivity might be associated with population‐dependent growth costs of reproduction. (iv) Heterozygosity can be a good indicator of short‐term, intraspecific responses to novel environmental change.

Population variation in density‐dependent growth, mortality and their trade‐off in a stream fish

“…After the fact, we can suggest three possible mechanisms. First, differences in life history characteristics for these populations, which may be under divergent selection (Fraser et al, 2018), can lead to different reaction norms to density (Wright, Bolstad, Araya-Ajoy, & Dingemanse, 2019). For example, populations that exhibit a slower pace-of-life (i.e.…”

Combining population genomics and forward simulations to investigate stocking impacts: A case study of Muskellunge (Esox masquinongy) from the St. Lawrence River basin

“…This result indicates that the supplementation effort does not translate into effective migration in the long term, which further supports our hypothesis that introduced individuals may have lower fitness than fish from the resident local populations. Lower fitness was expected given that maladaptive change that reduces fitness in the wild can be observed within just one captive generation (Araki et al, 2007, Christie et al 2012Fraser et al 2018). Here, eggs from adults were kept and reared in a hatchery fish farm and more than half of them were released as juveniles (5-27 cm in length, De LaFontaine, unpublished) so that selected traits in the hatchery can differ from those providing highest fitness in the wild (Frankham, 2008).…”

“…the use of a low number of individual for reproduction in supportive breeding programs Laikre & Ryman, 1996;Ryman & Laikre, 1991), genetic homogenization of wild populations (Araki & Schmid, 2010;Eldridge, Myers, & Naish, 2009;Eldridge & Naish, 2007;Lamaze, Sauvage, Marie, Garant, & Bernatchez, 2012;Perrier, Guyomard, Bagliniere, Nikolic, & Evanno, 2013) and ultimately, the loss of local adaption (Araki et al, 2009;Ford, 2002;Lynch & O'Hely, 2001). Loss of local adaptation may stem from the fact that selected traits in captive environments or any foreign stocking source may differ from those providing the highest fitness in the local environment (Fraser et al 2018). Following admixture (impacting genome-wide structure), and eventual introgression (in which allelic variants can be transferred from one differentiated population to another), such differences in selective values, together with higher genetic load in stocked populations can lead to outbreeding depression resulting from disruption of co-adapted gene complexes or from the breakup of epistatic interactions (Lynch, 1991;Tallmon, Luikart, & Waples, 2004).…”

Combining population genomics and forward simulations to investigate stocking impacts: A case study of Muskellunge (Esox masquinongy) from the St. Lawrence River basin

“…From a genetic standpoint, the potential negative impacts of stocking include the following: reduction in genetic diversity and effective population size due to the Ryman-Laikre effect (i.e., use of small numbers of individuals for breeding programs, Laikre & Ryman, 1996;Ryman & Laikre, 1991), genetic homogenization of wild populations (Araki & Schmid, 2010;Eldridge, Myers, & Naish, 2009;Eldridge & Naish, 2007;Lamaze, Sauvage, Marie, Garant, & Bernatchez, 2012;Perrier, Guyomard, Bagliniere, Nikolic, & Evanno, 2013), and ultimately the loss of locally adapted traits (Araki, Cooper, & Blouin, 2009;Ford, 2002;Lynch & O'Hely, 2001). Loss of local adaptation may arise from selection of traits associated with captive environments or because a divergent stocking source may exhibit reduced fitness in the local environment (Fraser et al, 2018). With admixture (impacting genomewide structure) and eventual introgression (where allelic variants are transferred from one differentiated population to another), differences in selective values can lead to outbreeding depression through disruption of co-adapted gene complexes or from the breakup of epistatic interactions (Lynch, 1991;Tallmon, Luikart, & Waples, 2004).…”