Age-dependent genetic architecture across ontogeny of body size in sticklebacks

Abstract

Heritable variation in traits under natural selection is a prerequisite for evolutionary response. While it is recognized that trait heritability may vary spatially and temporally depending on which environmental conditions traits are expressed under, less is known about the possibility that genetic variance contributing to the expected selection response in a given trait may vary at different stages of ontogeny. Specifically, whether different loci underlie the expression of a trait throughout development and thus providing an additional source of variation for selection to act on in the wild, is unclear. Here we show that body size, an important life-history trait, is heritable throughout ontogeny in the nine-spined stickleback ( Pungitius pungitius ). Nevertheless, both analyses of quantitative trait loci and genetic correlations across ages show that different chromosomes/loci contribute to this heritability in different ontogenic time-points. This suggests that body size can respond to selection at different stages of ontogeny but that this response is determined by different loci at different points of development. Hence, our study provides important results regarding our understanding of the genetics of ontogeny and opens an interesting avenue of research for studying age-specific genetic architecture as a source of non-parallel evolution.

Age-Dependent Growth-Related QTL Variations in Pacific Abalone, Haliotis discus hannai

“…None of the detected QTLs were expressed in all ages of Pacific abalone, which means there is no common QTL that affects growth traits at every age. A similar QTL variation in growth-related traits across ages was reported in fish and plants including the nine-spined stickleback [31] and radiata pine [25]. Further, the number of QTLs detected for each trait varied with age.…”

“…The present results demonstrate that the QTL expression for growth-related traits, such as BW, SL, and SW, were different across ages in Pacific abalone. Variations in QTL expression in growth-related traits at different ages have been reported in Scottish blackface sheep [24], the radiata pine [25], the nine-spined stickleback [31], chicken [32], mice [34], and the rubber tree [35]. None of the detected QTLs were expressed in all ages of Pacific abalone, which means there is no common QTL that affects growth traits at every age.…”

“…Growth-related QTL studies have been performed on several commercially important molluscan species, including the Pacific abalone [7,16], small abalone [26], blacklip abalone [27], Manila clam [28], Pacific oyster [29], and bay scallop [30]. On the other hand, QTL variations across ages and families have been reported in several mammals and fishes, including the gilthead seabream [23], blackface sheep [24], nine-spined stickleback [31], chicken [32], and common carp [33]. However, no report on QTL variations across ages in invertebrate species has been published.…”

Heterogeneous genomic architecture of skeletal armour traits in sticklebacks

“…Nevertheless, genomic heritabilities for standard length and body depth (h 2 = 0.21 -0.26) were very similar to the summed PVEs of individual QTL affecting these traits (0.11 -0.27), suggesting an oligogenic basis of body size variation. This inference is supported by biometric estimates which have yielded very similar heritabilities within (h 2 = 0.13 -0.18; Shimada et al 2011) and among (h 2 = 0.07 -0.25; Fraimout et al 2022) population crosses in nine-spined sticklebacks.…”

Dissecting the genetic architecture of quantitative traits using genome‐wide identity‐by‐descent sharing

“…Following the colonization of lakes and ponds from the marine environment, freshwater populations of P. pungitius have repeatedly evolved distinct phenotypes such as increased body size (i.e. gigantism; Herczeg et al., 2009a, 2009b), changes in behaviour (Herczeg et al., 2009a, 2009b, Fraimout, Li, et al., 2022), and pelvic reduction (Kemppainen et al., 2021a, 2021b). A reasonable assumption is therefore that sufficient additive genetic variance was available in the marine ancestral population to respond to the selection pressures associated with the colonization of the freshwater habitat.…”