The Role of Prolactin in the Regulation of Clutch Size and Onset of Incubation Behavior in the American Kestrel

doi:10.1006/hbeh.2000.1616

Hormones and Behavior

Volume 38, Issue 3, November 2000, Pages 168-176

https://doi.org/10.1006/hbeh.2000.1616 Get rights and content

Abstract

In most bird species, the timing of incubation onset may influence the degree of hatching asynchrony, which, together with variation in clutch size, affects reproductive success. In some domesticated species that usually show no hatching asynchrony, plasma prolactin concentrations in females rise with the onset of incubation and the end of laying, and this rise enhances incubation behavior and may terminate laying. To investigate whether a rise in prolactin during laying is involved in the regulation of clutch size and incubation onset in a species with hatching asynchrony, we measured plasma concentrations of immunoreactive prolactin (ir-prolactin) in laying American kestrels, Falco sparverius, and quantified clutch size and incubation behavior. In a separate study, we administered one of three concentrations of ovine prolactin (o-prolactin) via osmotic pumps implanted in females when egg 2 of a clutch was laid. ir-Prolactin concentrations during laying were higher in small than in large clutches and increased in parallel with the development of incubation behavior. o-Prolactin treatment enhanced incubation behavior, but did not affect clutch size, possibly because the manipulation was performed after clutch size had already been determined. Consistent with studies on domesticated species that show synchronous hatching, our results indicate that rising prolactin during laying enhances the expression of incubation behavior in a species that shows hatching asynchrony. Further studies are necessary to determine whether the relationship between prolactin and clutch size in the American kestrel is one of causation or of mere association.

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Further, experiments in doves show that systemic and intracerebroventricular (icv) PRL injections, at levels akin to those circulating during parental care, maintain parental responses and reduce gonad size and LH plasma levels (Buntin et al., 1991, 1988; Buntin and Tesch, 1985; Janik and Buntin, 1985). The evidence for an inhibitory effect of PRL on the HPG axis has been connected to its possible role in photorefractoriness (Dawson and Sharp, 1998), clutch size regulation (Ryan et al., 2015; Sockman et al., 2000) and parental care (Angelier et al., 2016; Buntin, 1996). In contrast, many other studies have not found evidence for such an anti-gonadal effect of PRL.
Prolactin, a hormone involved in vertebrate parental care, is hypothesized to inhibit reproductive hypothalamic-pituitary-gonadal (HPG) axis activity during parenting, thus maintaining investment in the current brood as opposed to new reproductive efforts. While prolactin underlies many parental behaviors in birds, its effects on other reproductive behaviors, such as courtship, remain unstudied. How prolactin affects neuropeptide and hormone receptor expression across the avian HPG axis also remains unknown. To address these questions, we administered ovine prolactin (oPRL) or a vehicle control to both sexes in experienced pairs of the biparental rock dove (Columba livia), after nest removal at the end of incubation. We found that oPRL promoted parental responses to novel chicks and stimulated crop growth compared to controls, consistent with other studies. However, we found that neither courtship behaviors, copulation rates nor pair maintenance differed with oPRL treatment. Across the HPG, we found oPRL had little effect on gene expression in hypothalamic nuclei, but increased expression of FSHB and hypothalamic hormone receptor genes in the pituitary. In the gonads, oPRL increased testes size and gonadotropin receptor expression, but did not affect ovarian state or small white follicle gene expression. However, the oviducts of oPRL-treated females were smaller and had lower estrogen receptor expression compared with controls. Our results highlight that some species, especially those that show multiple brooding, may continue to express mating behavior despite elevated prolactin. Thus, mechanisms may exist for prolactin to promote investment in parental care without concurrent inhibition of reproductive function or HPG axis activity.
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Although the concentrations of PRL are the highest during the brooding period in most cases (Buntin et al., 1996; Chastel et al., 2005), several studies also found that plasma PRL drops shortly after hatching and is maintained at a moderate level during the brooding period (Goldsmith, 1982; El Halawani et al., 1988). Additionally, some studies have found that temperature, food availability, breeding experience and breeding parameters would also affect hormone levels of birds (Silver et al., 1980; Cate et al., 1993; Sockman et al., 2000; Angelier et al., 2006; Silverin et al., 2008; Ouyang et al., 2011; Riechert et al., 2014; Ryan et al., 2014; Valle et al., 2015; Smiley and Adkins-Regan, 2016a,b). Therefore, the secretion patterns of LH and PRL may be different among breeding stages in different species over time.
The reproductive behaviors of birds are mainly controlled by the hypothalamus-pituitary-gonad axis. Many studies have shown that reproductive hormones are tightly linked to the breeding sub-stages. However, only a few studies have examined the temporal trend of hormone levels among different reproductive stages in multiple brooded species. We investigated the changes in plasma luteinizing hormone (LH) and prolactin (PRL) concentrations during different reproductive stages of the facultative double-brooded Great Tit (Parus major). We found that the concentrations of LH and PRL in females were significantly higher than those in males. Females had significantly higher LH and lower PRL concentrations in the pre-breeding period than in the first/second brooding periods, and there were no significant changes between the first and second brooding periods. The concentrations of LH and PRL in males had no significant difference between the pre-breeding period and the first brooding periods, while LH and PRL concentrations in the second brooding period were significantly higher than those in the first brooding period. We conclude that there are sex-based differences between LH and PRL at different stages of reproduction. The changes in LH and PRL in both males and females should be related to their physiological functions. Especially for males, individuals with higher levels of LH and PRL are more likely to maintain second clutches.
Prolactin and prolactin receptor expression in the HPG axis and crop during parental care in both sexes of a biparental bird (Columba livia)
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During breeding, multiple circulating hormones, including prolactin, facilitate reproductive transitions in species that exhibit parental care. Prolactin underlies parental behaviors and related physiological changes across many vertebrates, including birds and mammals. While circulating prolactin levels often fluctuate across breeding, less is known about how relevant target tissues vary in their prolactin responsiveness via prolactin receptor (PRLR) expression. Recent studies have also investigated prolactin (PRL) gene expression outside of the pituitary (i.e., extra-pituitary PRL), but how PRL gene expression varies during parental care in non-pituitary tissue (e.g., hypothalamus, gonads) remains largely unknown. Further, it is unclear if and how tissue-specific PRL and PRLR vary between the sexes during biparental care. To address this, we measured PRL and PRLR gene expression in tissues relevant to parental care, the endocrine reproductive hypothalamic-pituitary- gonadal (HPG) axis and the crop (a tissue with a similar function as the mammalian mammary gland), across various reproductive stages in both sexes of a biparental bird, the rock dove (Columba livia). We also assessed how these genes responded to changes in offspring presence by adding chicks mid-incubation, simulating an early hatch when prolactin levels were still moderately low. We found that pituitary PRL expression showed similar increases as plasma prolactin levels, and detected extra-pituitary PRL in the hypothalamus, gonads and crop. Hypothalamic and gonadal PRLR expression also changed as birds began incubation. Crop PRLR expression correlated with plasma prolactin, peaking when chicks hatched. In response to replacing eggs with a novel chick mid-incubation, hypothalamic and gonadal PRL and PRLR gene expression differed significantly compared to mid-incubation controls, even when plasma prolactin levels did not differ. We also found sex differences in PRL and PRLR that suggest gene expression may allow males to compensate for lower levels in prolactin by upregulating PRLR in all tissues. Overall, this study advances our understanding of how tissue-specific changes in responsiveness to parental hormones may differ across key reproductive transitions, in response to offspring cues, and between the sexes.
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Citation Excerpt :
Accordingly, several correlational and experimental studies highlighted the predominant role of prolactin in the set-up and maintenance of incubation behaviors (Angelier et al., 2016; Buntin, 1996; Lynn, 2016; Sockman et al., 2006; Vleck, 2002). For example, Sockman et al. (2000) demonstrated that a moderate experimental increase in prolactin concentration induces a better incubation commitment (i.e. percent day incubating) in American kestrels (Falco sparverius). Furthermore, previous research on kittiwakes from the same colony reported that experimentally induced low prolactin levels were associated with reduced nest attendance during the chick-rearing period (Angelier et al., 2009).
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Regular ArticleThe Role of Prolactin in the Regulation of Clutch Size and Onset of Incubation Behavior in the American Kestrel

Abstract

Trends Ecol. Evol.

Gen. Comp. Endocrinol.

Adv. Stud. Behav.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Theriogenology

Anim. Behav.

Anim. Behav.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Horm. Behav.

Gen. Comp. Endocrinol.

Trends Ecol. Evol.

Brain Res.

Gen. Comp. Endocrinol.

Anim. Behav.

Comp. Biochem. Physiol. C

Gen. Comp. Endocrinol.

Anim. Behav.

The bal-chatri: A trap for the birds of prey

Bird-Banding

Seasonality of clutch size determination in the kestrel Falco tinnunculus: An experimental approach

Ornis Scand.

Serum levels of luteinizing hormone, prolactin, estradiol and progesterone in laying and nonlaying mallards (Anas platyrhynchos)

Biol. Reprod.

Incubation behaviour and hatching patterns in the American kestrel Falco sparverius

Ornis Scand.

Prevention of the expression of incubation behaviour using passive immunisation against prolactin in turkey hens (Meleagris gallopavo)

Reprod. Nutr. Dev.

Incubation behavior in the domestic turkey: Physiological correlates

CRC Crit. Rev. Poult. Biol.

Hormonal induction of incubation behavior in ovariectomized female turkeys (Meleagris gallopavo)

Biol. Reprod.

Regular Article
The Role of Prolactin in the Regulation of Clutch Size and Onset of Incubation Behavior in the American Kestrel