Polygenic and major-locus contributions to sexual maturation timing in Atlantic salmon

Sexual maturation timing is a life-history trait central to the balance between mortality and reproduction. Maturation may be triggered when an underlying compound trait, called liability, exceeds a threshold. In many different species and especially fishes, this liability is approximated by growth and body condition. However, environmental vs. genetic contributions either directly or via growth and body condition to maturation timing remain unclear. Uncertainty exists also because the maturation process can reverse this causality and itself affect growth and body condition. In addition, disentangling the contributions of polygenic and major loci can be important. In many fishes, males mature before females, enabling the study of associations between male maturation and maturation-unbiased female liability traits. Using 40 Atlantic salmon families, longitudinal common-garden experimentation, and quantitative genetic analyses, we disentangled environmental from polygenic and major locus (vgll3) effects on male maturation, and sex-specific growth and condition. We detected polygenic heritabilities for maturation, growth, and body condition, and vgll3 effects on maturation and body condition but not on growth. Longitudinal patterns for sex-specific phenotypic liability, and for genetic variances and correlations between sexes suggested that early growth and condition indeed positively affected maturation initiation. However, towards spawning time, causality appeared reversed for males whereby maturation affected growth negatively and condition positively via both the environmental and genetic effects. Altogether, the results indicate that growth and condition are useful traits to study liability for maturation initiation, but only until maturation alters their expression, and that vgll3 contributes to maturation initiation via condition.Peer reviewe

Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon

A major goal in biology is to understand how evolution shapes variation in individual life histories. Genome-wide association studies have been successful in uncovering genome regions linked with traits underlying life history variation in a range of species. However, lack of functional studies of the discovered genotype-phenotype associations severely restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here, we report acis-regulatory mechanism whereby expression of alternative isoforms of the transcription co-factorvestigial-like 3(vgll3) associate with variation in a key life history trait, age at maturity, in Atlantic salmon (Salmo salar). Using a common-garden experiment, we first show thatvgll3genotype associates with puberty timing in one-year-old salmon males. By way of temporal sampling ofvgll3expression in ten tissues across the first year of salmon development, we identify a pubertal transition invgll3expression where maturation coincided with a 66% reduction in testicularvgll3expression. Thelatematuration allele was not only associated with a tendency to delay puberty, but also with expression of a rare transcript isoform ofvgll3pre-puberty. By comparing absolutevgll3mRNA copies in heterozygotes we show that the expression difference between theearlyandlatematurity alleles is largelycis-regulatory. We propose a model whereby expression of a rare isoform from thelateallele shifts the liability of its carriers towards delaying puberty. These results exemplify the potential importance of regulatory differences as a mechanism for the evolution of life history traits. Author summary Alternative life history strategies are an important source of diversity within populations and promote the maintenance of adaptive capacity and population resilience. However, in many cases the molecular basis of different life history strategies remains elusive. Age at maturity is a key adaptive life history trait in Atlantic salmon and has a relatively simple genetic basis. Using salmon age at maturity as a model, we report a mechanism whereby different transcript isoforms of the key age at maturity gene,vestigial-like 3(vgll3), associate with variation in the timing of male puberty. Our results show how gene regulatory differences in conjunction with variation in gene transcript structure can encode for complex alternative life histories.Peer reviewe

Altered trait variability in response to size-selective mortality

Changes in trait variability owing to size-selective harvesting have received little attention in comparison with changes in mean trait values, perhaps because of the expectation that phenotypic variability should generally be eroded by directional selection typical for fishing and hunting. We show, however, that directional selection, in particular for large body size, leads to increased body-size variation in experimentally harvested zebrafish (Danio rerio) populations exposed to two alternative feeding environments: ad libitum and temporarily restricted food availability. Trait variation may influence population adaptivity, stability and resilience. Therefore, rather than exerting selection pressures that favour small individuals, our results stress the importance of protecting large ones, as they can harbour a great amount of variation within a population, to manage fish stocks sustainably.Peer Reviewe

Altered trait variability in response to size-selective mortality

Changes in trait variability owing to size-selective harvesting have received little attention in comparison with changes in mean trait values, perhaps because of the expectation that phenotypic variability should generally be eroded by directional selection typical for fishing and hunting. We show, however, that directional selection, in particular for large body size, leads to increased body-size variation in experimentally harvested zebrafish (Danio rerio) populations exposed to two alternative feeding environments: ad libitum and temporarily restricted food availability. Trait variation may influence population adaptivity, stability and resilience. Therefore, rather than exerting selection pressures that favour small individuals, our results stress the importance of protecting large ones, as they can harbour a great amount of variation within a population, to manage fish stocks sustainably.Peer Reviewe

Size-at-age data

Size at ages 35 d - 200

Further methods and results from Altered trait variability in response to size-selective mortality

Changes in trait variability owing to size-selective harvesting have received little attention in comparison with changes in mean trait values, perhaps because of the expectation that phenotypic variability should generally be eroded by directional selection typical for fishing and hunting. We show, however, that directional selection, in particular for large body size, leads to increased body-size variation in experimentally harvested zebrafish (<i>Danio rerio</i>) populations exposed to two alternative feeding environments: <i>ad libitum</i> and temporarily restricted food availability. Trait variation may influence population adaptivity, stability and resilience. Therefore, rather than exerting selection pressures that favor small individuals, our results stress the importance of protecting large ones as they can harbor a great amount of variation within a population, to manage fish stocks sustainably