Introduction
Photorefractoriness was a major issue in all fowl before modern selection programmes as it limited breeding opportunities within the flock. It terminates the breeding season after a period of time on long day lengths, and is dissipated after exposure to short day lengths. Thus, it causes seasonality in birds such that offspring are hatched at a favourable time of the year to maximise the chances of survival. It is obligatory for birds that express the absolute form, such as the partridge (Siopes and Wilson, Reference SIOPES and WILSON1978) to be exposed to short days for photorefractoriness to be dissipated, but in some species photorefractoriness may be dissipated even if they are reared on long days, but the dissipation in this case occurs at a slower rate. For example, sexual maturity is delayed in broiler breeders with no previous exposure to short day lengths (Lewis et al., Reference LEWIS, BACKHOUSE and GOUS2004), and turkeys were found to return to lay spontaneously despite remaining on long days (Siopes, Reference SIOPES2005). These species are said to be ‘relatively photorefractory’. While age at sexual maturity is influenced by body weight, with birds acquiring photosensitivity earlier when reared on an accelerated growth curve (Dunn and Sharp, Reference DUNN and SHARP1990), there is no interaction between age at photostimulation and body weight (Ciacciariello and Gous, Reference CIACCIARIELLO and GOUS2005). Where selection pressures have focussed on egg production, such as in egg-type hybrids, photorefractoriness has been virtually eliminated (Morris et al., Reference MORRIS, SHARP and BUTLER1995). Therefore it appears that selection programmes with different foci have resulted in a range in the degree to which photorefractoriness is exhibited between and probably within different species. This review reports the population and gender responses to photoperiod in an attempt to better understand the flock response.
Population differences in response to light (or genetic control)
The flock response to photostimulation can be variable, despite uniformity in target body weight. For example, when commercial laying pullets younger than 15 weeks, or broiler breeder pullets younger than 19 weeks of age are photostimulated, sexual development is delayed in a proportion of birds, while being advanced in others, despite flock body weights being uniform and on target (Lewis et al., Reference LEWIS, MORRIS and PERRY2002; Lewis and Morris, Reference LEWIS and MORRIS2006; Lewis et al., Reference LEWIS, GOUS and MORRIS2007). Thus, when a flock is photostimulated after the first bird becomes photoresponsive, but before the whole flock has achieved photosensitivity, a bimodal frequency distribution of age at maturity will result from the advance in maturity of some birds and the delay in others (Lewis, Reference LEWIS2009). Although the overall flock response may be classified as relative photorefractoriness, turkey hens in a flock have been shown to exhibit varying degrees of this trait (Siopes and Proudman, Reference SIOPES and PROUDMAN2003). Near the end of a typical laying period, a flock of turkeys will consist of a variable mix of birds that are still photosensitive and laying, some of whom may have shown spontaneous recovery of photosensitivity during the laying period whilst others are photorefractory and have ceased to lay (Siopes, Reference SIOPES2001). This varied response allows the flock to be classified into groups of non-responders, partial responders and full responders (Siopes and Proudman, Reference SIOPES and PROUDMAN2003). The egg production of non-responders was reported not to differ from the untreated controls left on 16L:8D. Partial responders were those whose egg production declined by more than one standard deviation of the control group level, and full responders ceased egg production for at least seven days following the light treatment.
Differences in photoresponsiveness between turkey breeder hens, shown by differences in egg production, were not reflected in circulating levels of either luteinising hormone (LH) or prolactin (PRL) (Siopes and Proudman, Reference SIOPES and PROUDMAN2003), suggesting that the most photosensitive hens can maintain egg production with levels of LH low enough to terminate egg production in other hens. However, the authors did not preclude the possibility that alterations in the preovulatory LH surge may account for the differences in photoresponsiveness (Siopes and Proudman, Reference SIOPES and PROUDMAN2003).
Proudman (Reference PROUDMAN1998) showed that plasma PRL levels rise following long-day photostimulation. Although these levels may vary throughout the photo- and scotophases, it was shown that measurements of daytime levels accurately reflect the reproductive state of turkey hens, where levels are moderate in good layers and low in those that are photorefractory (Proudman, Reference PROUDMAN1998).
In White Guinea fowl given an increase in light before the breeding season in an attempt to obtain hatching eggs at an earlier age, egg production was initiated earlier than those not given the light increase, but the time taken to reach 50% production was lengthened (Davis and Penquite, Reference DAVIS and PENQUITE1942). This demonstrated the variability in those birds that responded early, whereas the initiation in egg production was much more uniform, but delayed, in those not given a precocious increase in light. While most Chukar Partridges remained photorefractory when held on 16L:8D, one bird did lay a few eggs without any previous short day exposure, inferring that the potential for genetic selection against photorefractoriness exists (Siopes and Wilson, Reference SIOPES and WILSON1978).
Because selection for egg production has inadvertently led to a loss in the exhibition of photorefractoriness, there is concern that selection against birds displaying photorefractoriness could lead to a more egg-type than a meat-type bird. However, Tyler and Gous (Reference TYLER and GOUS2011) demonstrated that the response to early photostimulation is heritable, and, at least in the F1 generation, there was no detrimental effect on 21 d broiler body weight. Another concern is that, with a loss in photorefractoriness, it may become more difficult to control the age at sexual maturity, However, because these birds would respond to lighting programmes from an earlier age, the control of sexual maturity should be improved, due to greater uniformity in the time of acquisition of photosensitivity (Lewis et al., Reference LEWIS, CIACCIARIELLO and GOUS2003). In birds that are no longer photorefractory, exposure to constant long days will not markedly delay sexual maturity (Lewis et al., Reference LEWIS, MORRIS and PERRY1998), but a programme of long days followed by short days can still delay sexual maturity in egg-type hybrids that are not photorefractory (Lewis and Morris, Reference LEWIS and MORRIS2006). Currently there is a problem with broiler breeder eggs being too large to set, especially at the end of the production cycle. Because overall egg size can be manipulated with the use of lighting programmes in the rearing period (Lewis and Morris, Reference LEWIS and MORRIS2006), it is likely that efforts would lean towards advancing the age at sexual maturity, achieved by photostimulation and controlling growth curves (Ciacciariello and Gous, Reference CIACCIARIELLO and GOUS2005), because this would reduce egg size throughout the laying period. Egg production in the later stages of the laying period will decline whether or not birds exhibit photorefractoriness but this is due to ageing of the reproductive tract and a reduction in the rate of recruitment or yellow-yolky follicles as well as an increased incidence of follicular atresia, internal ovulation and the production of membranous or soft shelled eggs (Williams and Sharp, Reference WILLIAMS and SHARP1978). So egg production may well be increased in broiler breeder flocks that do not exhibit photorefractoriness.
Gender differences in response to photoperiod
Although it seems unlikely that reproductive control mechanisms have evolved differently between the genders, there may be some benefit in the males becoming fertile before the females became reproductively active, especially as the reproductive cost in females is considerably higher than in males. However, selection strategies could be expected to differ between sexes. A male may be advantaged by being the first to breed, which could allow more time to seek additional mating partners, but from the female perspective, being the first to breed, while possibly enhancing fecundity, may expose her to more stressful weather conditions (Ball and Ketterson, Reference BALL and KETTERSON2008). It appears that the absence of photorefractoriness is an evolutionary adaptation to allow flexibility at the end of the breeding season in species living in tropical areas, where favourable conditions may persist (Beebe et al., Reference BEEBE, BENTLEY and HAU2005). Common Weaver males, also a tropical species, do not exhibit photorefractoriness, as sexual activity was maintained throughout the duration of the experiment (15 months) without testes regression or loss in breeding condition occurring (Thapliyal and Saxena, Reference THAPLIYAL and SAXENA1964). Ball and Ketterson (Reference BALL and KETTERSON2008), showed that avian females could be expected to respond differently to males considering aspects such as investment in an egg by the female as well as the time and energy required for parental care. In seasonal migratory species, where both sexes arrive simultaneously, and both contribute to building the nest, incubation of eggs and parental care, the response to the environment could be expected to be similar. Conversely, where males gather early in the breeding season to advertise, and females only visit for copulation, it could be expected that males could respond differently to females, as in species where the male migrates earlier and defends his territory in advance of females (Ball and Ketterson, Reference BALL and KETTERSON2008). Gender differences in the response to photoperiod have been suggested in the Spotted Antbird (Beebe et al., Reference BEEBE, BENTLEY and HAU2005) where follicle size in females did not show the same increase as testis size in males when both were photostimulated at the end of the breeding season. This could have been due to the small number of females tested, but could be that females cannot respond to a small increase in light in the same manner as males (Beebe et al., Reference BEEBE, BENTLEY and HAU2005).
While photorefractoriness in the male avian species has been demonstrated in species such as starlings (Dawson and Sharp, Reference DAWSON and SHARP1998) and bantams (Sreekumar and Sharp, Reference SREEKUMAR and SHARP1998), there are inconsistent findings regarding the expression of photorefractoriness in broiler breeder males. It was clear that rearing male broiler breeders on long days resulted in delayed sexual maturity and probably an earlier onset of adult photorefractoriness (Tyler and Gous, Reference TYLER and GOUS2008), but there was a variable response to early photostimulation to which some birds responded, whilst others exhibited a delay in sexual maturity (Tyler and Gous, Reference TYLER and GOUS2009). Birds in these experiments were weighed weekly and feed allocation adjusted to maintain body weights on the recommended breed targets in an attempt to remove any body weight effect. Providing male broiler breeders with a mid-cycle increase in photoperiod did appear to advance the onset of adult photorefractoriness, evident from a decline in testosterone concentration observed at 60 weeks of age; however, this decline was insufficient to affect sperm concentration or comb area (Tyler et al., Reference TYLER, LEWIS and GOUS2011).
While it is evident that female turkeys exhibit photorefractoriness (Siopes, Reference SIOPES2002) it is questionable whether male turkeys do so. Male turkeys maintained under constant long days exhibit precocious semen production (Polley et al., Reference POLLEY, SHOFFNER, BURGER and JOHNSON1962; Noirault et al., Reference NOIRAULT, BRILLARD and BAKST2006). An increase in both LH and testosterone was observed at about 18 weeks in males kept on both 16L:8D or 6L:16D from 10 until 29 weeks of age (Yang et al., Reference YANG, LONG, INPANBUTR and BACON1998). The turkey toms responded positively to early photostimulation (although lighting treatment for the first 10 weeks is unknown, but assumed to be 6L:16D) where 13 birds on the 16L:8D treatment were producing semen by 25 weeks whereas only four out of 14 males produced semen in the 6L:16D treatment group. If turkey toms exhibit juvenile photorefractoriness, it would be expected that the 6-h photoperiod should allow faster dissipation of photorefractoriness than the 16-h photoperiod and that there would be no response to 10-week photostimulation, which was not the case. Proudman and Siopes (Reference SIOPES2005) could not find evidence of photorefractoriness in turkey toms, because plasma prolactin levels were found to be low in turkey toms following photostimulation, unlike the increase observed in turkey females, thought to be associated with the onset of photorefractoriness (Proudman, Reference PROUDMAN1998). Thyroid hormone levels did not differ between females and males in this study, but varied to a greater extent in males with an apparent 2- to 3-week cyclical interval in restricted males, while full-fed males showed less variation.
Eitan and Soller (Reference EITAN and SOLLER2000), in a two-way selection experiment for high and low photoresponsiveness of birds with early or late onset of semen production after exposure to ‘suboptimal’ photoperiods, concluded that it is possible to alter photoresponsiveness by selection, and that selection for photoresponsiveness in males results in a correlated response in their female progeny. However, the photoperiods regarded as being suboptimal in their selection experiments (short photoperiods during rearing) have subsequently been found to be optimal for the dissipation of photorefractoriness (Lewis et al., Reference LEWIS, BACKHOUSE and GOUS2004). Because both the early and late maturing lines in their experiment showed a similar advance in mean age at onset of semen production, as well as the fact that the photoperiods used could not distinguish between birds that exhibited photorefractoriness or not, their results cannot be attributed to the heritability of photoresponsiveness. The experiment by Tyler and Gous (Reference TYLER and GOUS2011), where broiler breeder males were selected for early and late onset of semen production by rearing them on short days to eight weeks and then photostimulating them at that age, does however show that it is possible to select for photoresponsiveness: birds that were photorefractory did not respond to early photostimulation whereas female offspring from those that did respond exhibited an advance in age at first egg.
Implications for the poultry industry
If successful, genetic selection against juvenile photorefractoriness in broiler breeders would eliminate the considerable delay in the attainment of sexual maturity in ‘out-of-season’ flocks reared on long days (>14 h) in open-sided houses thereby increasing the number of eggs laid by birds reared under such conditions. This has already been successfully achieved in commercial laying stocks (Morris et al., Reference MORRIS, SHARP and BUTLER1995; Lewis and Morris, Reference LEWIS and MORRIS2006) and sufficient evidence now exists to show that this is possible among broiler breeders. Because the rate at which adult photorefractoriness develops is inversely related to the rate at which the juvenile form is dissipated (Lewis et al., Reference LEWIS, CIACCIARIELLO and GOUS2003), elimination of juvenile photorefractoriness would suggest that egg production and fertility in broiler breeder flocks might no longer decline as rapidly towards the end of the laying period. This would increase the potential laying performance of broiler breeders and would allow them to perform closer to this potential without production being constrained by long day lengths in rearing and lay, thereby maximising the number of fertile hatching eggs laid by each bird.
Acknowledgements
This material is based upon work supported financially by the National Research Foundation. Any opinion, findings and conclusions or recommendations expressed in this material are those of the authors and therefore the NRF does not accept any liability in regard thereto.
