Genetic and phenotypic responses to genomic selection for timing of breeding in a wild songbird

Abstract

The physiological mechanisms underlying avian seasonal timing of reproduction, a life‐history trait with major fitness consequences, are not well understood. Comparing individuals that have been selected to differ in their timing of breeding may prove to be a promising in studying these mechanisms, making selection lines a valuable tool. We created selection lines for early and late timing of breeding in great tits (Parus major) using genomic selection, that is selection based on multi‐marker genotypes rather than on the phenotype. We took in nestlings (F1 generation) from wild broods of which the mother was either an extremely early (“early line”) or extremely late (“late line”) breeder. These chicks were then genotyped and, based on their “genomic breeding values” (GEBVs), we selected individuals for early and late line breeding pairs to produce the F2 generation in captivity. The F2 offspring was hand‐reared, genotyped and selected to produce an F3 generation, which were then again genotyped and selected. This way we obtained laying dates in aviaries for F1, F2 and F3 birds. We studied the genetic response to the artificial selection and found increased genetic differentiation between the early and late reproducing selection lines over generations (F1–F3), indicated by both diverging GEBVs and increased fixation indices (FST). We studied the phenotypic response to selection for birds breeding in outdoor breeding aviaries. We found that early line birds laid earlier than late line birds, and this difference increased over the generations (F1–F3), with non‐significant line effects for the F1 and F2, but highly significant line differences for the F3. We also assessed whether there was correlated selection on two traits that are potentially part of the mechanisms underlying seasonal timing: the endogenous free‐running period of the day/night clock (tau) and basal metabolic rate, but found no correlated selection. We have successfully created selection lines on seasonal timing in a wild bird species and obtained an instrument for future studies to investigate the physiological mechanisms underlying timing of breeding, and the genetic variation in these mechanisms, an essential component for evolutionary change in timing of reproduction. A free Plain Language Summary can be found within the Supporting Information of this article.

Fine-tuning of seasonal timing of breeding is regulated downstream in the underlying neuro-endocrine system in a small songbird

“…The selection line study results are reported elsewhere (Verhagen et al, 2019). Briefly, we found that on average early-line birds laid their eggs about 6 days earlier than late-line birds.…”

“…Briefly, we found that on average early-line birds laid their eggs about 6 days earlier than late-line birds. Further, the difference in average laying date increased (from about 2 to 10 days) from the F 1 to the F 3 generation, with non-significant line effects for the F 1 and F 2 generation, but highly significant line differences for the F 3 generation (Verhagen et al, 2019).…”

“…Here, we used female great tits from selection lines where birds were genomically selected for either early or late timing of breeding (Gienapp et al, 2019;Verhagen et al, 2019). Birds were subjected to two contrasting temperature environments in climate-controlled aviaries.…”

Epigenetic mediation of the onset of reproduction in a songbird

“…We used the great tit, a well-known model species in ecology and evolution with a reference genome 25 , SNP arrays (10k 42 and 650k 43 ), and whole transcriptome and methylome for various tissues 25,41,44 . The individuals included are part of a bidirectional selection experiment for early and late reproduction using genomic selection 45,46 (details in methods S1). For the experiment, we housed 36 breeding pairs of the F2 generation in climate-controlled aviaries mimicking natural temperature and photoperiod patterns of a cold and warm year in the Netherlands 47,48 .…”

Quantifying evolution in wild populations

“…This is possible because laying date is a heritable (polygenic) trait (Van der Jeugd and McCleery 2002;. Such a selection experiment was recently completed in great tits (Parus major) originating from the Dutch Hoge Veluwe population (see Gienapp et al 2019;Verhagen et al in review for details of this selection experiment). Female offspring of birds that were selected to breed either early or late in outdoor aviaries exhibited extreme genomic breeding values and concomitant different phenotypes between early-and lateline birds in captivity (Verhagen et al in review).…”