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

Verhagen, Irene; Laine, Veronika N.; Mateman, A. Christa; Pijl, Agata; Wit, Ruben de; Lith, Bart van; Kamphuis, Willem; Viitaniemi, Heidi M.; Williams, Tony; Samuel, P.; Meddle, Simone; Gienapp, Phillip; Oers, Kees van; Visser, Marcel E.

doi:10.1242/jeb.202481

Cited by 14 publications

(21 citation statements)

References 78 publications

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“…In these aviaries, birds were subjected to two contrasting temperature treatments mimicking an extremely cold and extremely warm spring in the Netherlands. Laying dates of these females will be published elsewhere (I. Verhagen, V. N. Laine, A. C. Mateman, A. Pijl, R. de Wit, B. van Lith, M. E. Visser, Unpublished, I. Verhagen et al, in prep). It is, however, worth mentioning that the laying dates in these breeding pairs did not differ between the early and late selection lines, nor that an interaction was found between selection line and temperature treatment.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2019

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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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2019

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“…The climate-controlled aviaries have been described in detail elsewhere (Verhagen et al, 2019a) but, briefly, 36 pairs of the F 3 generation of the selection lines (see 'Selection lines in timing of breeding', above) were housed in 36 climate-controlled aviaries in January 2017. These birds had less extreme GEBVs (see above) compared with the birds housed in the outdoor aviaries.…”

Section: Climate-controlled Aviariesmentioning

confidence: 99%

“…In addition, two contrasting temperature treatments (Fig. 1A) were provided, mimicking an extreme cold (2013) or extreme warm (2014) spring in The Netherlands (for details, see Verhagen et al, 2019a). This was reflected in (average) egg-laying dates between these years in the Hoge Veluwe population, where females (n=47 for which we obtained laying dates for both 2013 and 2014) laid ∼24 days earlier in 2014 than in 2013 ( Fig.…”

Section: Climate-controlled Aviariesmentioning

confidence: 99%

Temperature has a causal and plastic effect on timing of breeding in a small songbird

Verhagen

Tomotani

Gienapp

et al. 2020

Journal of Experimental Biology

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Phenotypic plasticity is an important mechanism by which an individual can adapt its seasonal timing to predictable, short-term environmental changes by using predictive cues. Identification of these cues is crucial to forecast the response of species to long-term environmental change and to study their potential to adapt. Individual great tits (Parus major) start reproduction early under warmer conditions in the wild, but whether this effect is causal is not well known. We housed 36 pairs of great tits in climate-controlled aviaries and 40 pairs in outdoor aviaries, where they bred under artificial contrasting temperature treatments or in semi-natural conditions, respectively, for two consecutive years, using birds from lines selected for early and late egg laying. We thus obtained laying dates in two different thermal environments for each female. Females bred earlier under warmer conditions in climatecontrolled aviaries, but not in outdoor aviaries. The latter was inconsistent with laying dates from our wild population. Further, early selection line females initiated egg laying consistently ∼9 days earlier than late selection line females in outdoor aviaries, but we found no difference in the degree of plasticity (i.e. the sensitivity to temperature) in laying date between selection lines. Because we found that temperature causally affects laying date, climate change will lead to earlier laying. This advancement is, however, unlikely to be sufficient, thereby leading to selection for earlier laying. Our results suggest that natural selection may lead to a change in mean phenotype, but not to a change in the sensitivity of laying dates to temperature.

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“…While the physiological responses to the photoperiodic manipulation resulted in faster gonadal development, in the wild we did not find any advancement of the onset of egg laying. This suggests that photoperiod is necessary to trigger the physiological changes underlying reproduction, but that additional cues must be involved in the regulation of egg laying phenology, perhaps more at the level of the gonads and liver than at the level of the brain (Verhagen et al 2019).…”

Section: Discussionmentioning

confidence: 99%

Manipulation of photoperiod perception advances gonadal growth but not laying date in the great tit

Salis

Samuel

Hut

et al. 2019

Journal of Avian Biology

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In seasonal environments, organisms use biotic and abiotic cues to time various biological processes that are crucial for growth, survival and reproductive success. Photoperiod is the best‐known cue used to regulate gonadal development, migration and moult of many animal species. In birds, the relationship between photoperiod and gonadal development is clearly established, but we have little understanding on whether photoperiod also regulates actual timing of egg laying under natural conditions. Elucidating the link between photoperiod and timing of breeding is however key to understand whether an evolutionary change in sensitivity to photoperiod is a possible mechanism through which organisms could adjust their seasonal timing in response to climate warming. Here, we investigated the causal relationship between photoperiod, gonadal growth and laying date in wild female great tits. We experimentally increased the photoperiod perceived by the birds in spring by clipping head feathers, and we subsequently monitored gonadal development in the lab and egg laying dates in the wild. We show that our manipulation increased the photoperiod perceived by the birds to a level that approximately corresponds to an advancement of ten calendar days. This increase in perceived photoperiod led to an acceleration of gonadal development, but not to an advancement of egg laying dates. Our results indicate that photoperiod sensitivity is not constraining the advancement of laying date under current environmental conditions and suggest that evolution of sensitivity to other supplementary cues is necessary to advance reproduction under global warming.

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

Cited by 14 publications

References 78 publications

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

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

Temperature has a causal and plastic effect on timing of breeding in a small songbird

Manipulation of photoperiod perception advances gonadal growth but not laying date in the great tit

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