Time spent in distinct life history stages has sex‐specific effects on reproductive fitness in wild Atlantic salmon

Abstract

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a 4‐year pedigree to investigate if time spent in two distinct life history stages has sex‐specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW, measured in years), and years spent in the marine environment as adults (sea age, SW, measured in sea winters) on 264 sexually mature adults collected on a river spawning ground. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5,000 offspring). Sea age is significantly and positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: 62.2% increase in offspring/SW and 34.8% increase in mate number/SW; males: 201.9% offspring/SW and 60.3% mates/SW). Younger freshwater age was significantly related to older sea age and thus increased reproductive fitness, but only among females (females: −33.9% offspring/FW and −32.4% mates/FW). This result implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and more males returned at a younger age than females despite the reproductive fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex‐specific consequence on female reproductive fitness, demonstrating a life history trade‐off between maturation and reproduction in wild Atlantic salmon.

Life‐history genomic regions explain differences in Atlantic salmon marine diet specialization

“…, see also,Barson et al 2015). Given that larger size at a given sea age is indicative of higher performance and fitness in adult salmon (e.g.,Fleming 1996;Mobley et al 2020), the six6*L allele (being linked to larger size) may be expected to have a selective advantage over the E allele and is hence predicted to prevail within and among populations as a result of directional selection. However, the six6 genomic region is highly variable within and among populations(Barson et al 2015, Pritchard et al 2018, and balancing selection appears to be the pervasive mode of evolution, with both alleles exerting fitness advantage with different life-history strategies(Barson et al 2015).…”

Maturation in Atlantic salmon (Salmo salar, Salmonidae): a synthesis of ecological, genetic, and molecular processes

“…The age at smoltification has direct effects on sea age (Box 1) and reproductive fitness. Earlier smolting individuals tend to spend more time at sea before returning to rivers to spawn (Erkinaro et al, 2019;Jonsson & Jonsson, 2011;Salminen, 1997) and have higher reproductive fitness due to generally achieving larger size (Mobley et al, 2020). There may also be a sexspecific relationship between growth and time spent in fresh water.…”

“…For example, females that spend more time in fresh water show reduced pre-and post-smolt (Box 1) growth (Einum et al, 2002), signifying a trade-off between growth at sea and the time spent in fresh water. A recent study demonstrated that females that spend more time in fresh water spend less time at sea than earlier smolting individuals, and suffer a reduction in reproductive success (Mobley et al, 2020). However, smolting early potentially exposes these individuals to higher predation at sea, highlighting a potential tradeoff between smolting and survival (McCormick et al, 1998).…”

“…Marine survival of Atlantic salmon is size-and age-dependent with orders of magnitude higher mortality rates at the post-smolt stage, compared to older and larger adults (Chaput, Caron, & Marshall, 2003;Chaput et al, 2018;Michielsens et al, 2006). High mortality in the marine phase may confer a selective advantage to earlier maturation, such that higher probability of survival before reproduction may offset the advantage of being older and larger at maturity (Hard et al, 2008;Mobley et al, 2020;Thorpe, 2007).…”

“…Atlantic salmon commonly spend one to three years (but can be up to 5 years) in the marine environment before returning to fresh water to spawn for the first time (Jonsson & Jonsson, 2011;Webb et al, 2007). Every additional year in the marine environment results in doubling of individual mass; individuals returning after one year are typically 1-3 kg and 50-65 cm, compared to 10-20 kg and >100 cm after spending three or more years in the marine environment (Hutchings & Jones, 1998;Mobley et al, 2020). The main determinants of return migration timing are likely a mixture of the ecological factors, genetics, and the physiological state of the fish.…”