Abstract:Circannual rhythms regulate seasonal reproduction in many vertebrates. The present study investigated whether circannual reproductive phenotypes (rhythms in growth of gonads and molt) were generated independently of the circadian clocks in the subtropical non-photoperiodic spotted munia (Lonchura punctulata). Birds were subjected to light:dark (LD) cycles with identical light but varying dark hours, such that the period of LD cycle (T) equaled 16 h (T16; 12 h L:4 h D), 21 h (T21; 12 h L:9 h D), 24 h (T24; 12 h… Show more
“…The role of tau in circannual rhythms (such as seasonal timing) is, however, unclear. Although some studies did not find a link between circadian and circannual rhythms (Agarwal, Mishra, Komal, Rani, & Kumar, ; Budki, Malik, Rani, & Kumar, ), others have found evidence that they are linked (Gwinner, ; Myung et al, ). Therefore, we chose to investigate a possible response in tau in our breeding time selection lines.…”
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.
“…The role of tau in circannual rhythms (such as seasonal timing) is, however, unclear. Although some studies did not find a link between circadian and circannual rhythms (Agarwal, Mishra, Komal, Rani, & Kumar, ; Budki, Malik, Rani, & Kumar, ), others have found evidence that they are linked (Gwinner, ; Myung et al, ). Therefore, we chose to investigate a possible response in tau in our breeding time selection lines.…”
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.
“…Accordingly, we carried out the present study using subtropical spotted munia ( Lonchura punctulata ), which is an estrildid seasonal breeder with a reproductive season extending from July to October . In captivity, circannual cycles of gonadal maturation‐regression and moult have been shown to persist, regardless of the duration of the light or dark period, or the absence of light or darkness altogether: constant darkness (DD) or light (LL) . However, an interaction of the circannual rhythm with the photoperiodic cycle is necessary to synchronise breeding to the calendar year in the wild .…”
Section: Introductionmentioning
confidence: 99%
“…In captivity, circannual cycles of gonadal maturation‐regression and moult have been shown to persist, regardless of the duration of the light or dark period, or the absence of light or darkness altogether: constant darkness (DD) or light (LL) . However, an interaction of the circannual rhythm with the photoperiodic cycle is necessary to synchronise breeding to the calendar year in the wild . Spotted munia appear to use small increments of 1.5‐2 minutes of daily photoperiod changes around the vernal equinox to synchronise their reproductive cycle to the calendar year .…”
Section: Introductionmentioning
confidence: 99%
“…When exposed to constant photoperiods (eg 12:12 hour light/dark cycle [12L:12D] or 24:24 hour light/dark cycle [24L:24D]) or to constant light (LL) for about 2 years, circannual testicular and ovarian cycles persisted with a period of 11 months and 10‐13 months, respectively . Similarly, postnuptial moult was found more dispersed in females than in males under these light conditions …”
Section: Introductionmentioning
confidence: 99%
“…Therefore, we expected (i) a correlation of OPN5 expression with the length of the light period, namely low and high OPN5 mRNA and protein levels under long night (eg, 3L:21D) and long day (eg, 21L:3D), respectively; (ii) high GnRH‐I/NPY and low GnIH/VIP mRNA and protein levels under 3L:21D, and vice versa under 21L:3D; and (iii) high DIO2/ low DIO3 mRNA levels under 3L:21D, and vice versa under 21L:3D. We also expected a sex‐difference in expression patterns, in view of reported differences in the circannual gonadal and moult cycles between male and female spotted munias …”
Circannual rhythm regulates the annual timing of reproduction in spotted munia, with sex differences in its relationship with the external photoperiod environment. Interestingly, munia show an atypical photosensitivity and exhibit gonadal maturation when acutely exposed to an unnatural short photoperiod (eg 3 hours of light per day; ie a long scotoperiod). The proximate mechanisms regulating scotoperiod-induced hypothalamic-pituitary-gonadal (HPG) activation are unclear. Because thyroid hormone signalling plays a central role in photoperiodic induction, we hypothesised the involvement of similar mechanism, comprising alterations in hypothalamic deiodinases, under long scotoperiod-induced HPG activation. To test this, several endpoints of cellular and molecular correlates were assayed in male and female munias after 1 and 4 weeks of exposure to an 3:21 hour light/dark cycle (3L:21D), with controls on a 21:3 hour light/dark cycle (21L:3D). We measured the hypothalamic expression of mRNA and protein of light-sensitive (neuropsin, OPN5) and reproductive (vasoactive intestinal peptide [VIP], neuropeptide Y [NPY], gonadotrophin-releasing hormone [GnRH], gonadotrophin-inhibiting hormone [GnIH]) neuropeptides by quantitative polymerase chain reaction (PCR) and immunohistochemistry, respectively. In addition, we also measured mRNA expression of types 2 (DIO2) and 3 (DIO3) deiodinases that regulate triiodothyronine-mediated GnRH release and gonadal maturation in photoperiodic species. The quantitative PCR and immunohistochemistry results were consistent. Higher OPN5 levels under 21L:3D than under 3L:21D suggested its role in sensing the length of the light period. Similarly, low VIP and high NPY expression under 3L:21D than under 21L:3D were consistent with their roles as cellular correlates of photic and nonphotic environment, respectively. High GnRH-I/low GnIH levels and gonadal recrudescence under 3L:21D, and an inverse pattern under 21L:3D, confirmed the scotostimulation of HPG axis in spotted munia. However, DIO2 and DIO3 mRNA levels did not differ between 2 scotoperiods, in contrast to their reciprocal expression pattern found during long-day photostimulation. We demonstrate for the first time sex-dependent scotostimulation of reproductive neural pathways and suggest the involvement of molecules other than hypothalamic deiodinases in the regulation of gonad development cycle in 'nonphotoperiodic' seasonally breeding vertebrates.
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