Multigenerational hybridisation and its consequences for maternal effects in Atlantic salmon

Abstract

Outbreeding between segregating populations can be important from an evolutionary, conservation and economical-agricultural perspective. Whether and how outbreeding influences maternal effects in wild populations has rarely been studied, despite both the prominent maternal influence on early offspring survival and the known presence of fitness effects resulting from outbreeding in many taxa. We studied several traits during the yolk-feeding stage in multigenerational crosses between a wild and a domesticated Atlantic salmon (Salmo salar) population up to their third-generation hybrid in a common laboratory environment. Using cross-means analysis, we inferred that maternal additive outbreeding effects underlie most offspring traits but that yolk mass also underlies maternal dominant effects. As a consequence of the interplay between additive and dominant maternally controlled traits, offspring from first-generation hybrid mothers expressed an excessive proportion of residual yolk mass, relative to total mass, at the time of first feeding. Their residual yolk mass was 23-97% greater than those of other crosses and 31% more than that predicted by a purely additive model. Offspring additive, epistatic and epistatic offspring-bymaternal outbreeding effects appeared to further modify this largely maternally controlled cross-means pattern, resulting in an increase in offspring size with the percentage of domesticated alleles. Fitness implications remain elusive because of unknown phenotype-by-environment interactions. However, these results suggest how mechanistically co-adapted genetic maternal control on early offspring development can be disrupted by the effects of combining alleles from divergent populations. Complex outbreeding effects at both the maternal and offspring levels make the prediction of hybrid phenotypes difficult.

Early life traits of farm and wild Atlantic salmon Salmo salar and first generation hybrids in the south coast of Newfoundland

“…In contrast, in Debes et al . () all domesticated dam offspring appeared to have a faster yolk‐sac conversion efficiency. Although there seems to be a genetic component to growth prior to the onset of exogenous feeding (Solberg et al ., ), together, results of these studies as well as the findings here suggest no clear pattern in terms of domestication effect on the rate of early endogenous resource utilization.…”

“…When the female ID factor was explored, results show an effect of individual mothers irrespective of their origin on most larval traits. This is in accordance with previous farm–wild interaction studies where strong individual maternal effects were detected for early‐life offspring traits (Debes et al ., ; Bicskei et al ., ). There is a significant interaction, however, between cross type and female ID showing a different female effect within cross types suggesting potential male effects as well.…”

Half a century of genetic interaction between farmed and wild Atlantic salmon: Status of knowledge and unanswered questions

“…In addition, the competitive balance between farmed and wild salmon may differ with environmental conditions (Fraser et al., ; Harvey, Glover et al., ; Solberg, Zhang et al., ). In addition, the response of F1 hybrids and different backcross types may not always manifest in an additive manner (Debes et al., ; Einum & Fleming, ; Houde et al., ), and differs among populations (Einum & Fleming, ; Houde et al., ). Finally, variation in differences in egg size among the invading farmed escapees and the specific wild population will also influence the competitive balance and potential consequences.…”

“…One can also compensate or account for variations in body size in the data analyses (Debes & Hutchings, ; Glover et al., ), manipulate growth of the farmed or wild salmon by changing temperature and or feed rations or use a combination of approaches such as investigating both size‐matched individuals and age‐matched individuals to reduce potential bias (as has been made in the case of a rainbow trout ( Oncorhynchus mykiss , Salmonidae) domestication study) (White, Sakhrani, Danzmann, & Devlin, ). Alternatively, experiments can be conducted on the very early life‐history stages (Bicskei, Bron, Glover, & Taggart, ; Debes, Fraser, McBride, & Hutchings, ; Fraser, Minto, Calvert, Eddington, & Hutchings, ; Solberg et al., ) before intrinsic growth differences lead to differences in size. However, while the latter represents the most “unbiased approach,” it obviously limits measurements to early life‐history stages.…”

Effects of domestication on parr maturity, growth, and vulnerability to predation in Atlantic salmon

“…We did not record any data for these early stages, as we expect a confounding of among-strain differences with strain-specific maternal environmental effects. Maternal environmental effects in salmon are strongest during the egg stage, cease towards first feeding (Debes et al 2013), and continuously decrease thereafter (Heath et al 1999).…”