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Feed intake regulation for the female broiler breeder: In theory and in practice1,2
©2010 Poultry Science Association, Inc.
Feed intake regulation for the female broiler breeder: In theory and in practice1,2 M. P. Richards,*3 R. W. Rosebrough,* C. N. Coon,† and J. P. McMurtry* *USDA, Agricultural Research Service, Animal Biosciences and Biotechnology Laboratory, Beltsville, MD 20705-2350; and †University of Arkansas, Center of Excellence for Poultry Science, Fayetteville 72701
SUMMARY The modern commercial broiler is the product of intensive genetic selection for rapid and efficient growth. An unintended consequence of this selective breeding has been the loss of the ability for self-regulation of feed intake to closely match the requirements for maintenance, growth, and reproduction. Thus, the broiler tends to overconsume feed, resulting in a range of metabolic and health problems related to the development of obesity. These problems progress with age and become a significant impediment to the production of parent stock. To manage this situation, broiler breeder birds must be subjected to severe feed restriction, beginning early in life, to ensure that appropriate BW and composition are achieved at critical phases of the production cycle. This review focuses on the female broiler breeder because this bird requires the most intensive management with respect to feed allocation throughout production to attain BW targets that ensure good livability and efficient egg and chick production. Background information is provided on the cellular and molecular mechanisms that regulate feed intake and energy expenditure in poultry. In addition, several examples are discussed with regard to the endocrine and metabolic consequences of different feeding regimens commonly used in the management of the female breeder during the rearing and egg-laying phases of production. Key words: broiler breeder, energy balance, feed restriction, feeding regimen, obesity 2010 J. Appl. Poult. Res. 19:182–193 doi:10.3382/japr.2010-00167
DESCRIPTION OF PROBLEM The modern broiler breeder female is the product of intensive genetic selection for 2 important but conflicting criteria, rapid and efficient growth and a high rate of egg production [1]. Selection for increased juvenile BW and en1
hanced meat yield in broilers has also resulted in a disproportional increase in voluntary feed intake. Unlike layers that are able to self-regulate their feed intake to closely match the energy requirements for maintenance, growth, and reproduction, modern broilers, if given unrestricted access to feed, will overconsume well beyond
Presented as part of the Informal Nutrition Symposium at the Poultry Science Association’s 98th annual meeting in Raleigh, North Carolina, July 20–23, 2009. 2 Mention of a trade name, proprietary product, or specific equipment does not constitute a guarantee or warranty by USDA and does not imply its approval to the exclusion of other suitable products. 3 Corresponding author: [email protected]
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Primary Audience: Researchers, Nutritionists, Primary Breeders, Broiler Breeder Producers
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physiological and metabolic consequences of feed restriction regimens that are currently being used in commercial female breeder management programs.
MECHANISMS REGULATING FEED INTAKE IN POULTRY The mechanisms regulating feed intake in poultry involve more than mere appetite control. Therefore, it is necessary to consider the underlying relationships between energy status and basic physiological processes that require energy, such as maintenance, growth, and reproduction. Body weight is set throughout the life cycle by coordinated adjustments to feed intake and energy expenditure. Specific mechanisms have evolved to sense cellular and wholebody energy status. These sensing mechanisms are coupled with unique signaling pathways that link peripheral tissues where energy is utilized or stored with the central nervous system (CNS), which regulates energy acquisition via control of feed intake. Although some aspects of the regulation of feed intake by the CNS and peripheral tissues in birds have been reviewed previously [5–11], our understanding of the cellular and molecular mechanisms that integrate feed intake regulation with energy sensing in poultry remains quite limited. In fact, most of the discoveries concerning the regulation of appetite and energy expenditure have come from studies involving mammalian species. Because feeding and energy homeostasis are fundamental actions necessary for survival, it is logical to assume that the regulatory mechanisms governing these processes would be highly conserved in all animals [6, 7]. However, it is also clear that there are distinct functional differences in feed intake regulation between birds and mammals [8–11]. This section discusses some of the emerging concepts of feed intake regulation in birds, with the objective of providing new insights into determining how this process might have been altered in the broiler breeder by decades of genetic selection for broiler growth and meat production traits. Short- and Long-Term Regulation The drive to feed ensures that immediate nutritional requirements are met. Appetite control
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what is needed to achieve energy homeostasis. As a result, they soon reach a state of positive energy balance, which progresses with advancing age. Although the negative effects of chronic positive energy balance are largely avoided in broilers raised to market BW, breeding stock are much more susceptible. Adult BW and composition are adversely affected, and breeder birds inevitably succumb to a range of metabolic and reproductive problems linked to the development of obesity if they are not carefully managed throughout the production cycle. Efficient reproduction, health, and livability of the female breeder hen must be maintained while retaining all the genetic potential for rapid and efficient juvenile growth and high meat yield to be passed on to the next generation of broilers. However, it has been clearly shown that growth and reproductive fitness are negatively related production traits [2]. Therefore, effective management of the commercial broiler breeder inevitably involves a compromise. Body weight gain must be limited throughout production of these birds by reducing feed intake to minimize the occurrence of reproductive problems in the adult bird. This situation constitutes what has been referred to as the “broiler breeder paradox” [3]. That is, the seemingly impossible task of producing a bird that retains all the important broiler production traits while severely restricting its feed intake to limit BW gain. Continued selection pressure for increased juvenile BW gain and enhanced meat yield in the broiler will only further contribute to this dilemma by creating a bird that is increasingly unfit to survive as an adult [1, 4]. Thus, ad libitum feeding during rearing and egg production of female broiler breeders is no longer feasible. Instead, the producer must intervene early on by limiting the allocation of feed to attain specifically targeted BW profiles that seek to maximize reproductive fitness at sexual maturity. However, such intervention comes at a cost in terms of management and perceived welfare issues [1, 4]. To better understand how this situation has developed and what might be done in response, it is necessary to consider what is known about feed intake regulation in birds. This review provides background information concerning cellular and molecular mechanisms for regulating voluntary feed intake in poultry and explores some of the
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Signaling Molecules A variety of signaling molecules are produced by peripheral and CNS tissues in response to changes in nutritional status. Included among these are neuropeptides, hormones, nutrients, and metabolites. For each of these signaling molecules to be active, specific sensors that recognize and bind them must be produced at sites of action. Sensors can be transmembrane receptors, enzymes, transcription factors, and transporters. Together, each signal and its cognate sensor form a signaling pathway that can produce localized effects within individual cells and tissues, or they can work globally on the whole-body level via actions in the CNS [10]. Scanes [12] recently reviewed the functions of the major hormones required to support normal growth in birds, which include growth hormone, triiodothyronine (T3), and insulin-like growth factor-I (IGF-I). Insulin, glucagon, and corticosterone are the major hormones that control tissue metabolism. Each of these signaling molecules responds to changes in nutritional status, and each requires a set-point concentration in circulation to achieve optimal growth and tissue metabolism mediated by signaling through its cognate receptor. The different peptide hormones that have been identified and studied in poultry with respect to their effects on feed intake are presented
in Table 1. Although many of these molecules are highly conserved, their function can sometimes be different in birds as compared with mammals [8–11]. Ghrelin, a peptide hormone produced by the proventriculus, is an example of a signaling molecule that functions differently in birds, despite the fact that the structure and sequence of the ghrelin peptide and those of its receptor (growth hormone secretagogue receptor) are highly conserved. In mammals, ghrelin is a potent stimulator of appetite, whereas in birds, it strongly inhibits feed intake when administered centrally. Other examples of peptides exhibiting a different function in birds compared with mammals are included in Table 1. Another important aspect of signaling molecules concerns those produced specifically by adipose tissue. These molecules are referred to as adipokines or adipocytokines, and the discovery and subsequent characterization of leptin has highlighted an important role for adipose tissue as an endocrine organ. In Table 2 are listed some adipokine molecules that may be produced by adipose tissue in birds, although as of yet there have been no studies to systematically identify and characterize avian adipose-derived peptides. Adipokines exhibit a wide range of functions, including roles in feed intake regulation (e.g., leptin), insulin sensitivity (e.g., adiponectin), cardiovascular function (plasminogen activator inhibitor-1), and inflammation and immune function (e.g., IL-6). Moreover, individual adipokines such as leptin can have multiple actions on such processes as feed intake, ovarian maturation, bone remodeling, and tissue lipid metabolism. Some adipokines (e.g., leptin) are produced in proportion to the size of adipose tissue and thus act to signal the amount of body energy stores. Adipokines also play key roles in triggering the physiological and metabolic dysfunction that accompanies the development of obesity. Therefore, the amount of adipose tissue accumulated during growth and development is likely to be an important factor in determining the overall health and fertility of poultry. Energy-Sensing and Metabolic Programming The ability to sense energy status and adjust metabolic pathway activity in response is a basic function of cells in all animal species [13]. En-
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is thus crucial to ensuring optimal nutrition and achieving full potential for growth and development in poultry. Control of feed intake in the short term (i.e., meal to meal) involves hormonal and neural signals originating mainly in the gut that are generated in response to the presence of feed or specific nutrients. Over the longer term, the level of body energy stored primarily in the form of lipid in adipose tissue is closely monitored. Adaptive changes in feed intake, digestion, absorption, and metabolism work together to maintain whole-body energy balance and BW in response to a constantly changing external environment. In addition to meeting immediate energy demands, feed intake can also be adjusted to ensure that energy is stored in anticipation of periods of high demand, such as egg production, or to compensate for periods of feed shortage or deprivation so as to maintain BW.
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Table 1. Peptide hormone signals associated with feed intake regulation in birds Peptide hormone
Orexigenic (stimulate)
Neuropeptide Y Agouti-related protein Peptide YY1 Pancreatic polypeptide1 Galanin Visfatin1
No effect
Melanin concentrating hormone1 Orexins (A and B)1 Motilin1
Anorexigenic (inhibit)
α-Melanocyte-stimulating hormone Cocaine- and amphetamine-regulated transcript Corticotropin-releasing factor Growth hormone-releasing hormone1 Leptin Ghrelin1 Insulin Glucagon Glucagon-like peptide 1 Cholecystokinin Bombesin Gastrin Urotensin I, urocortin Neuromedin U/S
1
Indicates a different effect in birds as compared with mammals.
ergy-sensing pathways are present in the CNS and peripheral tissues of birds, and they represent another set of regulatory mechanisms that are used to modulate peripheral tissue metabolic activity as well as regulate feed intake and energy expenditure to maintain energy balance and BW [10].
The AMP-activated protein kinase (AMPK) is a highly conserved energy sensor (an enzyme) that also regulates cellular metabolism [14, 15, and the references therein]. The AMPK is a serine-threonine kinase and a central component of a kinase signaling cascade that is a critical control point for maintaining energy homeosta-
Table 2. Potential adipokines produced by avian adipose tissue Adipokine
Proposed functions
Leptin Adiponectin Visfatin
Feed intake regulation, ovarian maturation, hepatic lipogenesis, bone remodeling Modulator of insulin sensitivity and energy homeostasis Feed intake regulation, B cell growth factor, NAD metabolism, glucose and fatty acid metabolism, insulin mimetic Resistin Innate immune response, inflammation, insulin resistance Adipsin Complement D-like molecule, serine protease Acylation-stimulating protein Fatty acid reesterification and triglyceride storage, lipolysis Adiponutrin Energy homeostasis IL-6 Acute phase inflammatory response, energy metabolism Tumor necrosis factor family (TNF-α-like1) Proinflammatory cytokine Transforming growth factor-β Regulation of cell cycle Plasminogen activator inhibitor-1 Serine protease inhibitor, blood clotting Apelin Cardiovascular function Angiotensinogen Cardiovascular function, vasoconstriction 1
Chickens do not have a TNF-α gene homolog.
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nutrient availability with tissue growth and development. Central and Peripheral Regulatory Pathways Coordinated regulation of feed intake and energy expenditure responds to external environmental cues (feed availability, feed composition, photoperiod, temperature, stressors) and internal physiological signals (hormone, nutrient, and metabolite levels). The brain, and the hypothalamus in particular, plays a pivotal role in interpreting all this information and generating the appropriate responses in feed intake and energy expenditure to maintain energy homeostasis [10]. The hypothalamic melanocortin system comprises the crucial feeding regulatory neural circuitry and is composed of 2 populations of neurons, one set that expresses neuropeptide Y (NPY) and agouti-related protein (AgRP) and a second set that expresses proopiomelanocortin (POMC), a precursor containing α-melanocyte-stimulating hormone. Stimulation of NPY/AgRP-expressing (anabolic) neurons mediates a net increase in feed intake and energy storage, whereas stimulation of the POMC-expressing (catabolic) neurons results in a net decrease in energy intake and storage. Activation of AMPK in the hypothalamus in response to lowered energy status stimulates activity of the NPY/AgRP-expressing (anabolic) neurons and thus leads to increased feed intake and reduced energy expenditure, which work together to increase energy status. Conversely, activation of mTOR causes increased activity of the POMCexpressing (catabolic) neurons, which in turn causes a reduction in feed intake and increased energy expenditure, thereby promoting the utilization of energy for maintenance, growth, and reproduction. Thus, balance in the activity of hypothalamic melanocortin system neurons is what ultimately determines whole-body energy balance and BW. Changes in the circulating levels of leptin and insulin signal the hypothalamus to bring about long-term changes in energy balance by activating or inhibiting specific hypothalamic neurons. Leptin acts on the melanocortin system within the hypothalamus, either directly or indirectly, to reduce feed intake in chickens [17]. Similarly,
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sis on both the cellular and whole-body levels. The AMPK is activated by metabolic and environmental stresses that deplete cells of energy (i.e., adenosine triphosphate). The activity of AMPK is modulated by nutrient (e.g., glucose, fatty acids) and hormonal (e.g., leptin, ghrelin, insulin, adiponectin) signals in key peripheral tissues involved in nutrient partitioning and energy metabolism (liver, skeletal muscle, and adipose tissue) as well as in neurons in specific regulatory sites within the CNS. Once activated, AMPK works to inhibit energy-consuming (anabolic) pathways such as carbohydrate, lipid, and protein synthesis while stimulating energyproducing (catabolic) pathways such as the oxidation of glucose and fatty acids. These actions are accomplished by regulating the activity and expression levels of key metabolic enzymes controlling cellular metabolism. Another important fuel-sensing kinase pathway involves the mammalian target of rapamycin (mTOR), a serine-threonine kinase complex that also responds to nutrient (e.g., amino acids) and hormonal (e.g., leptin, insulin) signaling. Like AMPK, mTOR responds to changes in energy status. However, unlike AMPK, mTOR is activated in response to elevated energy status [10]. Moreover, activation of AMPK leads to the inactivation of mTOR. In response to elevated energy status, mTOR stimulates the rate of cellular protein synthesis, growth, and proliferation commensurate with increased nutrient availability. Thus, AMPK and mTOR have overlapping but opposite functions with respect to controlling metabolic activity in response to changes in energy supply [10]. Activities of the lipid, carbohydrate, and protein metabolic pathways in the CNS and peripheral tissues are coordinately regulated by both AMPK and mTOR [10]. The AMPK controls the activity of acetyl-coenzyme A carboxylase (ACC), the rate-limiting enzyme in fatty acid biosynthesis in liver, and thus plays a key role in the modulation of lipid storage in adipose tissue [15]. The mTOR plays an important role in insulin-induced protein synthesis in skeletal muscle and is therefore an important factor in determining the growth of this tissue [16]. The combined actions of the AMPK and mTOR kinase pathways represent a regulatory mechanism linking
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THE IMPACT OF SELECTION ON FEED INTAKE REGULATION GENES Surprisingly, only a few systematic efforts have been reported that identify and characterize specific feed intake regulatory component genes in peripheral tissues and CNS in broilers as compared with other types of birds. Successful identification of such genes and the changes in their expression would provide potential genetic markers that may be useful in marker-assisted selection programs to address the problems affecting broiler breeders as well as to provide new insights into the genetic basis for regulating voluntary feed intake. In a comparison of layer and broiler chicks, Yuan et al. [19] reported that there were no differences in the expression of hypothalamic neuropeptides, including NPY, AgRP, POMC, and orexin, between the 2 groups at 7 d posthatch, despite the fact that BW and feed intake were already markedly different at this age. Similarly, the expression of associated genes such leptin receptor, ACC, and fatty acid synthase was also similar between the 2 groups in the hypothalamus. However, broiler chicks expressed higher levels of the glucocorticoid receptor in the hypothalamus, which was associated with lower levels of corticotrophin-releasing hormone expression. This could account for increased feed
intake in broilers. They also found higher expression of the fat mass and obesity-associated gene in broiler chicks as compared with layer chicks. The latter findings provide possible candidate marker genes, although that remains to be confirmed and validated. Byerly et al. [20] used cDNA microarrays and individual gene expression analysis to assess differential expression of anabolic/orexigenic and catabolic/anorexigenic genes in hypothalamic samples from fat and lean selected chicken lines. They reported that interactions between the neuropeptide brainderived neurotrophic factor and the hormones T3 and corticosterone might constitute a mechanism linking hypothalamic energy regulation with body composition by controlling expression of specific CNS obesity network genes, including leptin receptor, POMC, NPY, AgRP, and thyroid-releasing hormone. Ka et al. [21] compared 2 populations of chickens selected for BW at 56 d of age (selected for high and low weight) using cDNA microarray technology to determine differences in gene expression in a portion of the brain (diencephalon) containing the major metabolic regulatory regions, including the hypothalamus and brain stem. No definitive changes in expression of major regulatory components (i.e., neuropeptides and receptors) were detected and only small changes were found in genes thought to regulate neuronal plasticity and lipid metabolism. Thus, no specific candidate genes were identified, suggesting that the extreme differences in BW phenotypes were the net result of small contributions from multiple genes. The authors further suggested that selection over many generations for increased juvenile BW in chickens had caused CNS function to adapt at different rates posthatch in the 2 groups, and this may account for the observed differences in feeding behavior. There has been some investigation using transcriptional profiling of liver tissue from lean vs. fat and fast- vs. slow-growing selected lines of broiler chickens to identify differentially expressed genes [22, 23]. Generally, these studies highlighted differences in metabolic enzymes and transcription factors, suggesting those genes as possible candidates for further study. These findings emphasize the importance of coordinately regulated metabolic pathways, such as
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insulin administered directly into the brain inhibits feed intake in chickens, and the anorexia produced in response to insulin signaling is associated with increased expression of POMC, cocaine- and amphetamine-regulated transcript, and corticotrophin-releasing hormone genes in the hypothalamus [18]. These effects may also involve an insulin-mediated increase in hypothalamic mTOR activity. Because plasma levels of both leptin and insulin rise and fall with increases and decreases in energy status, such as during fasting and refeeding in broilers, it is possible that these 2 key metabolic hormones could serve as peripheral signals of energy storage to the CNS in birds [10]. In doing so, they would be expected to play an important role in modulating hypothalamic melanocortin neural activity to produce appropriate changes in feed intake and energy expenditure to achieve energy homeostasis.
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FEED RESTRICTION IN FEMALE BROILER BREEDER MANAGEMENT The central difficulty associated with the management of modern female broiler breeder strains involves the inability of these birds to adequately self-regulate feed intake during growth and development to achieve an optimal BW and composition needed to support efficient egg and chick production by the hen. Therefore, female breeders are subjected to a high degree of feed restriction early in life. It has been suggested that the 7- to 15-wk period of the pullet growth phase is the most critical period for limiting BW increase and thus represents the phase of production requiring the highest degree of feed restriction [26]. In fact, during the rearing phase, feed allocation can be reduced by as much as one-third of the intake of ad libitum-fed birds of the same age or approximately one-half that of birds at the same BW [27]. To achieve better flock uniformity in commercial breeder produc-
tion, skip-a-day (SKP), 5–2, or 4–3 programs are often used in preference to providing a restricted amount of feed on an every-day (ED) basis [28]. Because of the severity of feed restriction imposed during the pullet phase of production, concerns continue to be raised about the effects on bird welfare [1]. However, the benefits of feed restriction to performance of the breeder hen are well known and include reduced BW, delayed sexual maturity, improved ovarian function with fewer multiple ovulations, higher egg production with better persistence and longer sequences, reduced numbers of abnormal eggs, and lower mortality during the laying period [1]. These observations support the need for feed restriction in the management of the broiler breeder because they demonstrate clear production benefits that outweigh the health problems associated with the development of obesity in unrestricted birds. Attempts to moderate or alleviate the need for feed restriction through the use of diet dilution (i.e., qualitative restriction) or the introduction of alternative genotypes, such as those containing the dwarf gene, have produced mixed results with respect to maintaining female breeder production efficiency [3]. Thus, a nonrestrictive feed management solution that balances production and welfare concerns does not appear to be a realistic possibility [1]. Because primary breeders maintain the selection pressure for increased juvenile growth rate and efficiency in subsequent generations of broilers, the divergence between broiler and broiler breeder BW targets continues to widen. As a result, the intensity of feed restriction will continue to increase to sustain adequate reproductive efficiency in the breeder female [4]. To date, there have been only a few reports concerning the physiological and metabolic consequences of restricted feeding in the female broiler breeder. In light of the previous discussion of energy signaling and sensing mechanisms used to regulate feed intake in birds, it is important to determine the impact of feed restriction on innate regulatory mechanisms to better assess the implications for overall health and well-being of the managed bird. The following brief discussion focuses on what is currently known about the impact of feed restriction regimens currently in use on hormonal and metabolic profiles in the female breeder.
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the lipogenic pathway in liver, as critical control points for maintaining whole-body energy balance. More studies are required to fully understand the genetic changes related to the control of feed intake and energy expenditure that have accompanied intensive selection of the modern broiler. One likely comparison that has not yet been undertaken, but that would provide highly relevant information, is to compare randombred (unselected) broiler strains with modern highly selected ones. Such a comparison was performed by Havenstein et al. [24] to demonstrate a 4.6fold increase in growth rate between 1957 and 2001. Moreover, they reported that only 10 to 15% of the 6-fold improvement in carcass yield was accounted for by nutritional changes, with 85 to 90% of the increase attributable to genetics [25]. The application of new functional genomic techniques to analyze key tissues (brain, liver, skeletal muscle, gut, adipose tissue) from such populations would yield highly useful information concerning what has changed in response to selection for growth and meat yield in the modern broiler. This is especially relevant for the genes involved in feed intake and energy homeostatic regulatory mechanisms. Clearly, this is an area that merits further study.
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ED feed allocation regimen with some degree of relaxation of the restriction. Whether the differences between ED and SKP feeding during the rearing period continue to affect birds after sexual maturity is unclear but merits further investigation. Without any feed restriction from hatch, breeder females can achieve a BW more than twice that of restricted-fed birds at the time of photostimulation, with double the amount of carcass fat at peak egg production [31, 32]. Because voluntary feed intake naturally declines and approaches ad libitum levels after BW reaches a plateau [31], ad libitum feeding before photostimulation has been evaluated as a means to allow for enhanced nutrition to meet the needs for egg production and to relax the feed restriction. However, a rapid rate of BW gain at sexual maturity has also been shown to decrease egg production [1]. Figure 1 shows the concentrations of 4 major metabolic hormones (insulin, leptin, T3, and IGF-I) in plasma from breeder females switched to ad libitum feeding at 21 wk of age (1 wk before photostimulation) or maintained on an ED feeding regimen through the plateau period of egg production. The levels of insulin and leptin were elevated in the birds fed ad libitum, especially before and just after photostimulation at 22 wk in the critical period leading to sexual maturity (i.e., first egg) [33, 34]. Changes in circulating hormones such as insulin and leptin signal the status of energy storage (i.e., abdominal fat pad size) and, in conjunction with T3, they also help regulate hepatic metabolic programs such as lipogenesis, which is a key determinant of energy storage in the bird. The ad libitum-fed breeders demonstrated increased hepatic expression of the ACC gene, which persisted throughout egg production (Figure 2). Similar findings were also noted for the expression of other lipogenic genes in the liver of ad libitum vs. restricted birds [33]. Changes in hepatic lipogenic enzyme gene expression were accompanied by increases in fat pad size and ovary weight compared with restricted-fed birds (Figure 2). These processes are linked and coordinately regulated in the breeder hen. Reduced total egg production and an increased number of abnormal eggs in response to ad libitum feeding were observed [33]. Together these
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There have been 2 recent reports comparing the effects of commonly used feed-restriction regimens during the rearing phase, ED vs. SKP, on plasma hormones and metabolites and on hepatic lipid metabolism in pullets at 16 wk of age [29, 30]. Periods without feed in the SKP birds resulted in a variety of changes in the plasma hormone and metabolite profiles. These changes included increased thyroxine, corticosterone, and glucagon. Plasma free fatty acid (nonesterified free fatty acid) levels increased during fasting (period without feed) as a result of lipid mobilization to provide energy, and lipid mobilization was likely stimulated by the increase in glucagon. Plasma insulin, T3, IGF-I, and triglyceride levels were reduced in SKP compared with ED birds, whereas plasma IGF-II levels appeared less responsive to feed deprivation. In general, the 2 feeding regimens produced marked changes in endocrine and metabolite profiles despite the fact that an identical amount of feed was consumed over time by both groups. The differential effects on metabolism were most likely the result of the unique changes in hormonal signaling that accompanied the 2 restriction regimens. Skipping 24-h periods of feeding, as is practiced in SKP, 5–2, or 4–3 programs, is believed to set up a state of repeated fasting-refeeding cycles [27]. Such a condition is thought to affect overall metabolic efficiency because of the constant need to store and release greater quantities of nutrients than if they were provided on a regular (ED) basis. Because the storage and mobilization of nutrients is not a totally efficient process, such nutrient turnover likely accounts for the reduced efficiency of the SKP vs. ED birds [27]. The findings that SKP caused more dramatic increases in the expression of the liver lipogenic genes ACC, fatty acid synthase, and malic enzyme compared with ED reflects a greater fluctuation in nutrient and energy supply caused by the recurring 24-h periods without feed [29]. The benefits of improved flock uniformity associated with SKP programs must be carefully weighed against the potential savings in feed cost and possible improvements in performance and efficiency attainable by using ED programs [27]. At or just before sexual maturity, most broiler breeders are typically switched to an
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Figure 1. Plasma levels of the major metabolic hormones insulin, leptin, triiodothyronine (T3), and insulin-like growth factor-I (IGF-I) in female broiler breeders fed ad libitum (Ad Lib) or maintained in feed restriction from 21 wk of age (Restricted). Plasma samples were collected before photostimulation (prelight, 22 wk), after photostimulation (postlight, 24.5 wk), at first egg, and at the plateau of egg production (36.5 wk). All values represent the mean ± SEM of 21 (pre- and postlight) or 40 (first egg and plateau) analyses. Different letters (a–f) designate significant differences (P < 0.05). Data depicted are from Sun et al. [34].
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findings emphasize the benefits of maintaining feed restriction (i.e., ED regimen) throughout the egg-laying period. Previously, it was shown that the multiple hierarchies and erratic ovulation that accompany ad libitum feeding of breeders are associated with abnormal regulation of follicle maturation and steroidogenesis in the ovary [1]. It is possible that increased circulating leptin levels observed in ad libitum-fed breeders affected ovarian follicular maturation because the levels of leptin receptor are upregulated in these birds during maturation of large yellow follicles [35]. Furthermore, administration of leptin to laying hens is known to advance sexual maturation by increasing follicular development and reducing apoptosis [36]. Therefore, it is possible that leptin could play a significant role in ovarian dysfunction in ad libitum-fed breeder hens [35]. However, an association between abdominal fat pad size (i.e., source of leptin) and the potential effects of leptin on ovarian function remains to be shown in birds. Moreover, defining a role for leptin in ovarian function is complicated by the controversy over the existence of the avian leptin gene [10]. Solving the controversy surrounding
this hormone will greatly aid our understanding of the potential role(s), if any, of leptin in avian biology. Changes in plasma IGF-I observed between restricted and ad libitum-fed breeders (Figure 1) could also have potential effects on the ovary because this growth factor is known to play an important localized role in ovarian function [37]. In summary, different feeding regimens used during the rearing and egg-laying phases of production have important effects on hormonal levels and key metabolic pathways in the female broiler breeder. Understanding the links between feed management and the consequent effects on hormones and metabolism will aid producers in meeting the nutritional requirements of birds at different phases of production through better feed management practices.
CONCLUSIONS AND APPLICATIONS
1. Feed restriction has now become an important and indispensable management tool for female broiler breeder production. How feed allocation is managed can have a significant impact on female
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Figure 2. Analysis of mRNA expression for the acetyl-coenzyme A carboxylase (ACC) gene in liver from female broiler breeders fed ad libitum (Ad Lib) or maintained in feed restriction from 21 wk of age (Restricted). Also shown are the corresponding relative abdominal fat pad and ovary weights. Values represent the mean ± SEM of 5 determinations for ACC gene expression and 21 (pre- and postlight) or 40 (first egg and plateau) for liver and ovary weight analyses. Different letters (a–d) designate significant differences (P < 0.05). Data depicted are from Richards et al. [33] and Sun et al. [34].
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REFERENCES AND NOTES 1. Renema, R. A., and F. E. Robinson. 2004. Defining normal: Comparison of feed restriction and full feeding of female broiler breeders. World’s Poult. Sci. J. 60:508–522.
2. Siegel, P. B., and E. A. Dunnington. 1985. Reproductive complications associated with selection for broiler growth. Pages 59–72 in Poultry Genetics and Breeding, W. G. Hill, J. M. Manson, and D. Hewitt, ed. British Poultry Science Ltd., Harlow, UK. 3. Decuypere, E., P. M. Hocking, K. Tona, O. Onagbesan, V. Bruggeman, E. K. M. Jones, S. Cassy, N. Rideau, S. Metayer, Y. Jego, J. Putterflam, S. Tesseraud, A. Collin, M. Duclos, J. J. Trevidy, and J. Williams. 2006. Broiler breeder paradox: A project report. World’s Poult. Sci. J. 62:443– 453. 4. Renema, R. A., M. E. Rustad, and F. E. Robinson. 2007. Implications of changes to commercial broiler and broiler breeder body weight targets over the past 30 years. World’s Poult. Sci. J. 63:457–471. 5. Denbow, D. M. 1994. Peripheral regulation of food intake in poultry. J. Nutr. 124:1349S–1354S. 6. Kuenzel, W. J. 1994. Central neuroanatomical systems involved in the regulation of food intake in birds and mammals. J. Nutr. 124:1355S–1370S. 7. Kuenzel, W. J., M. M. Beck, and R. Teruyama. 1999. Neural sites and pathways regulating food intake in birds: A comparative analysis to mammalian systems. J. Exp. Zool. 283:348–364. 8. Furuse, M. 2002. Central regulation of food intake in the neonatal chick. Anim. Sci. J. 73:83–94. 9. Richards, M. P. 2003. Genetic regulation of feed intake and energy balance. Poult. Sci. 82:907–916. 10. Richards, M. P., and M. Proszkowiec-Weglarz. 2007. Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poult. Sci. 86:1478–1490. 11. Furuse, M., H. Yamane, S. Tomonaga, Y. Tsuneyoshi, and D. M. Denbow. 2007. Neuropeptidergic regulation of food intake in the neonatal chick: A review. Jpn. Poult. Sci. 44:349–356. 12. Scanes, C. G. 2009. Perspectives on the endocrinology of poultry growth and metabolism. Gen. Comp. Endocrinol. 163:24–32. 13. Lindsley, J. E., and J. Rutter. 2004. Nutrient sensing and metabolic decisions. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 139:543–559. 14. Proszkowiec-Weglarz, M., M. P. Richards, R. Ramachandran, and J. P. McMurtry. 2006. Characterization of the AMP-activated protein kinase pathway in chickens. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 143:92– 106. 15. Proszkowiec-Weglarz, M., and M. P. Richards. 2007. 5′-AMP-Activated protein kinase in avian biology. Avian Poult. Biol. Rev. 18:123–145. 16. Duchêne, S., S. Métayer, E. Audouin, K. Bigot, J. Dupont, and S. Tesseraud. 2008. Refeeding and insulin activate the AKT/p70S6 kinase pathway without affecting IRS1 tyrosine phosphorylation in chicken muscle. Domest. Anim. Endocrinol. 34:1–13. 17. Dridi, S., Q. Swennen, E. Decuypere, and J. Buyse. 2005. Mode of leptin action in chicken hypothalamus. Brain Res. 1047:214–223. 18. Honda, K., H. Kamisoyama, T. Saneyasu, K. Sugahara, and S. Hasegawa. 2007. Central administration of insulin suppresses food intake in chicks. Neurosci. Lett. 423:153– 157. 19. Yuan, L., Y. Ni, S. Barth, Y. Wang, R. Grossmann, and R. Zhao. 2009. Layer and broiler chicks exhibit similar hypothalamic expression of orexigenic neuropeptides but
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breeder performance. This will become even more important as the selection pressure for increased growth and meat yield is increased with successive generations of broilers. 2. There is a need for more information concerning the underlying changes to feed intake regulatory genes brought about by intensive selection of broilers for growth and meat yield to provide a rational scientific basis to improve future selection indices for more efficient birds that are not adversely affected as adults. 3. There is likely going to be no good solution to the broiler breeder paradox. Continuing changes to commercial broiler and broiler breeder BW targets over the past 3 decades emphasize the increasingly difficult situation for relaxing or even eliminating feed restriction as a management tool for female broiler breeder management to address welfare concerns [4]. Target weights are not static, and they are constantly changing with changes in genetics of commercial birds. In fact, it is no longer clear what a “normal” BW is for the modern meattype parent stock because current growth curve BW targets are based on optimizing reproductive efficiency and not on achieving full genetic growth potential [1]. 4. It is now generally recognized that caloric restriction can improve health, mitigate metabolic disease, and prolong the lifespan in model organisms such as the worm, fly, and mouse [38]. This may actually be true in commercially raised poultry as well. The goal would be to develop feeding regimens such that the increasing genetic potential for growth is more precisely matched with the caloric demand so as to promote health and well-being in the female broiler breeder.
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29. de Beer, M., R. W. Rosebrough, B. A. Russell, S. M. Poch, M. P. Richards, and C. N. Coon. 2007. An examination of the role of feeding regimens in regulating metabolism during the broiler breeder grower period. 1. Hepatic lipid metabolism. Poult. Sci. 86:1726–1738. 30. de Beer, M., J. P. McMurtry, D. M. Brocht, and C. N. Coon. 2008. An examination of the role of feeding regimens in regulating metabolism during the broiler breeder grower period. 2. Plasma hormones and metabolites. Poult. Sci. 87:264–275. 31. Katanbaf, M. N., E. A. Dunnington, and P. B. Siegel. 1989. Restricted feeding in early and late feathering chickens. 1. Growth and physiological responses. Poult. Sci. 68:344–351. 32. Yu, M. W., F. E. Robinson, and A. R. Robblee. 1992. Effect of feed allowance during rearing and breeding on female broiler breeders. 1. Growth and carcass characteristics. Poult. Sci. 71:1739–1749. 33. Richards, M. P., S. M. Poch, C. N. Coon, R. W. Rosebrough, C. M. Ashwell, and J. P. McMurtry. 2003. Feed restriction significantly alters lipogenic gene expression in broiler breeder chickens. J. Nutr. 133:707–715. 34. Sun, J. M., M. P. Richards, R. W. Rosebrough, C. M. Ashwell, J. P. McMurtry, and C. N. Coon. 2006. The relationship of body composition, feed intake, and metabolic hormones for broiler breeder females. Poult. Sci. 85:1173– 1184. 35. Cassy, S., S. Metayer, S. Crochet, N. Rideau, A. Collin, and S. Tesseraud. 2004. Leptin receptor in the chicken ovary: Potential involvement in ovarian dysfunction of ad libitum-fed broiler breeder hens. Reprod. Biol. Endocrinol. 2:72. 36. Paczoska-Eliasiewicz, H. E., M. ProszkowiecWeglarz, J. Proudman, T. Jacek, M. Mika, A. Sechman, J. Rzasa, and A. Gertler. 2006. Exogenous leptin advances puberty in domestic hen. Domest. Anim. Endocrinol. 31:211– 226. 37. Onagbesan, O., V. Bruggeman, and E. Decuypere. 2009. Intra-ovarian growth factors regulating ovarian function in avian species. Anim. Reprod. Sci. 111:121–140. 38. Spindler, S. R. 2009. Biological effects of calorie restriction: From soup to nuts. Ageing Res. Rev. doi:10.1016/j. arr.2009.10.003.
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distinct expression of genes related to energy homeostasis and obesity. Brain Res. 1273:18–28. 20. Byerly, M. S., J. Simon, E. Lebihan-Duval, M. J. Duclos, L. A. Cogburn, and T. E. Porter. 2009. Effects of BDNF, T3, and corticosterone on expression of the hypothalamic obesity gene network in vivo and in vitro. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296:R1180–R1189. 21. Ka, S., J. Lindberg, L. Stromstedt, C. Fitzsimmons, N. Lindqvist, J. Lundeberg, P. B. Siegel, L. Andersson, and F. Hallbook. 2009. Extremely different behaviors in high and low body weight lines of chicken are associated with differential expression of genes involved in neuronal plasticity. J. Neuroendocrinol. 21:208–216. 22. Cogburn, L. A., X. Wang, W. Carre, L. Rejto, S. E. Aggrey, M. J. Duclos, J. Simon, and T. E. Porter. 2004. Functional genomics in chickens: Development of integrated-systems microarrays for transcriptional profiling and discovery of regulatory pathways. Comp. Funct. Genomics 5:253–261. 23. Bourneuf, E., F. Herault, C. Chicault, W. Carre, S. Assaf, A. Monnier, S. Mottier, S. Lagarrigue, M. Douaire, J. Mosser, and C. Diot. 2006. Microarray analysis of differential gene expression in liver of lean and fat chickens. Gene 372:162–170. 24. Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003. Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1500–1508. 25. Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003. Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1509–1518. 26. Bruggeman, V., O. Onagbesan, E. D’Hondt, E. Buys, M. Safri, D. Vanmontfort, L. Berghman, F. Vandesande, and E. Decuypere. 1999. Effects of timing and duration of feed restriction during rearing on reproductive characteristics in broiler breeder females. Poult. Sci. 78:1424–1434. 27. de Beer, M., and C. N. Coon. 2007. The effect of different feed restriction programs on reproductive performance, efficiency, frame size, and uniformity in broiler breeder hens. Poult. Sci. 86:1927–1939. 28. Cobb-Vantress. 2005. Cobb 500 Breeder Management Guide, Blueprint for Success. Cobb-Vantress, Siloam Springs, AR.
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Feed intake regulation for the female broiler breeder: In theory and in practice1,2 M. P. Richards,*3 R. W. Rosebrough,* C. N. Coon,† and J. P. McMurtry* *USDA, Agricultural Research Service, Animal Biosciences and Biotechnology Laboratory, Beltsville, MD 20705-2350; and †University of Arkansas, Center of Excellence for Poultry Science, Fayetteville 72701
SUMMARY The modern commercial broiler is the product of intensive genetic selection for rapid and efficient growth. An unintended consequence of this selective breeding has been the loss of the ability for self-regulation of feed intake to closely match the requirements for maintenance, growth, and reproduction. Thus, the broiler tends to overconsume feed, resulting in a range of metabolic and health problems related to the development of obesity. These problems progress with age and become a significant impediment to the production of parent stock. To manage this situation, broiler breeder birds must be subjected to severe feed restriction, beginning early in life, to ensure that appropriate BW and composition are achieved at critical phases of the production cycle. This review focuses on the female broiler breeder because this bird requires the most intensive management with respect to feed allocation throughout production to attain BW targets that ensure good livability and efficient egg and chick production. Background information is provided on the cellular and molecular mechanisms that regulate feed intake and energy expenditure in poultry. In addition, several examples are discussed with regard to the endocrine and metabolic consequences of different feeding regimens commonly used in the management of the female breeder during the rearing and egg-laying phases of production. Key words: broiler breeder, energy balance, feed restriction, feeding regimen, obesity 2010 J. Appl. Poult. Res. 19:182–193 doi:10.3382/japr.2010-00167
DESCRIPTION OF PROBLEM The modern broiler breeder female is the product of intensive genetic selection for 2 important but conflicting criteria, rapid and efficient growth and a high rate of egg production [1]. Selection for increased juvenile BW and en1
hanced meat yield in broilers has also resulted in a disproportional increase in voluntary feed intake. Unlike layers that are able to self-regulate their feed intake to closely match the energy requirements for maintenance, growth, and reproduction, modern broilers, if given unrestricted access to feed, will overconsume well beyond
Presented as part of the Informal Nutrition Symposium at the Poultry Science Association’s 98th annual meeting in Raleigh, North Carolina, July 20–23, 2009. 2 Mention of a trade name, proprietary product, or specific equipment does not constitute a guarantee or warranty by USDA and does not imply its approval to the exclusion of other suitable products. 3 Corresponding author: [email protected]
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Primary Audience: Researchers, Nutritionists, Primary Breeders, Broiler Breeder Producers
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physiological and metabolic consequences of feed restriction regimens that are currently being used in commercial female breeder management programs.
MECHANISMS REGULATING FEED INTAKE IN POULTRY The mechanisms regulating feed intake in poultry involve more than mere appetite control. Therefore, it is necessary to consider the underlying relationships between energy status and basic physiological processes that require energy, such as maintenance, growth, and reproduction. Body weight is set throughout the life cycle by coordinated adjustments to feed intake and energy expenditure. Specific mechanisms have evolved to sense cellular and wholebody energy status. These sensing mechanisms are coupled with unique signaling pathways that link peripheral tissues where energy is utilized or stored with the central nervous system (CNS), which regulates energy acquisition via control of feed intake. Although some aspects of the regulation of feed intake by the CNS and peripheral tissues in birds have been reviewed previously [5–11], our understanding of the cellular and molecular mechanisms that integrate feed intake regulation with energy sensing in poultry remains quite limited. In fact, most of the discoveries concerning the regulation of appetite and energy expenditure have come from studies involving mammalian species. Because feeding and energy homeostasis are fundamental actions necessary for survival, it is logical to assume that the regulatory mechanisms governing these processes would be highly conserved in all animals [6, 7]. However, it is also clear that there are distinct functional differences in feed intake regulation between birds and mammals [8–11]. This section discusses some of the emerging concepts of feed intake regulation in birds, with the objective of providing new insights into determining how this process might have been altered in the broiler breeder by decades of genetic selection for broiler growth and meat production traits. Short- and Long-Term Regulation The drive to feed ensures that immediate nutritional requirements are met. Appetite control
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what is needed to achieve energy homeostasis. As a result, they soon reach a state of positive energy balance, which progresses with advancing age. Although the negative effects of chronic positive energy balance are largely avoided in broilers raised to market BW, breeding stock are much more susceptible. Adult BW and composition are adversely affected, and breeder birds inevitably succumb to a range of metabolic and reproductive problems linked to the development of obesity if they are not carefully managed throughout the production cycle. Efficient reproduction, health, and livability of the female breeder hen must be maintained while retaining all the genetic potential for rapid and efficient juvenile growth and high meat yield to be passed on to the next generation of broilers. However, it has been clearly shown that growth and reproductive fitness are negatively related production traits [2]. Therefore, effective management of the commercial broiler breeder inevitably involves a compromise. Body weight gain must be limited throughout production of these birds by reducing feed intake to minimize the occurrence of reproductive problems in the adult bird. This situation constitutes what has been referred to as the “broiler breeder paradox” [3]. That is, the seemingly impossible task of producing a bird that retains all the important broiler production traits while severely restricting its feed intake to limit BW gain. Continued selection pressure for increased juvenile BW gain and enhanced meat yield in the broiler will only further contribute to this dilemma by creating a bird that is increasingly unfit to survive as an adult [1, 4]. Thus, ad libitum feeding during rearing and egg production of female broiler breeders is no longer feasible. Instead, the producer must intervene early on by limiting the allocation of feed to attain specifically targeted BW profiles that seek to maximize reproductive fitness at sexual maturity. However, such intervention comes at a cost in terms of management and perceived welfare issues [1, 4]. To better understand how this situation has developed and what might be done in response, it is necessary to consider what is known about feed intake regulation in birds. This review provides background information concerning cellular and molecular mechanisms for regulating voluntary feed intake in poultry and explores some of the
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Signaling Molecules A variety of signaling molecules are produced by peripheral and CNS tissues in response to changes in nutritional status. Included among these are neuropeptides, hormones, nutrients, and metabolites. For each of these signaling molecules to be active, specific sensors that recognize and bind them must be produced at sites of action. Sensors can be transmembrane receptors, enzymes, transcription factors, and transporters. Together, each signal and its cognate sensor form a signaling pathway that can produce localized effects within individual cells and tissues, or they can work globally on the whole-body level via actions in the CNS [10]. Scanes [12] recently reviewed the functions of the major hormones required to support normal growth in birds, which include growth hormone, triiodothyronine (T3), and insulin-like growth factor-I (IGF-I). Insulin, glucagon, and corticosterone are the major hormones that control tissue metabolism. Each of these signaling molecules responds to changes in nutritional status, and each requires a set-point concentration in circulation to achieve optimal growth and tissue metabolism mediated by signaling through its cognate receptor. The different peptide hormones that have been identified and studied in poultry with respect to their effects on feed intake are presented
in Table 1. Although many of these molecules are highly conserved, their function can sometimes be different in birds as compared with mammals [8–11]. Ghrelin, a peptide hormone produced by the proventriculus, is an example of a signaling molecule that functions differently in birds, despite the fact that the structure and sequence of the ghrelin peptide and those of its receptor (growth hormone secretagogue receptor) are highly conserved. In mammals, ghrelin is a potent stimulator of appetite, whereas in birds, it strongly inhibits feed intake when administered centrally. Other examples of peptides exhibiting a different function in birds compared with mammals are included in Table 1. Another important aspect of signaling molecules concerns those produced specifically by adipose tissue. These molecules are referred to as adipokines or adipocytokines, and the discovery and subsequent characterization of leptin has highlighted an important role for adipose tissue as an endocrine organ. In Table 2 are listed some adipokine molecules that may be produced by adipose tissue in birds, although as of yet there have been no studies to systematically identify and characterize avian adipose-derived peptides. Adipokines exhibit a wide range of functions, including roles in feed intake regulation (e.g., leptin), insulin sensitivity (e.g., adiponectin), cardiovascular function (plasminogen activator inhibitor-1), and inflammation and immune function (e.g., IL-6). Moreover, individual adipokines such as leptin can have multiple actions on such processes as feed intake, ovarian maturation, bone remodeling, and tissue lipid metabolism. Some adipokines (e.g., leptin) are produced in proportion to the size of adipose tissue and thus act to signal the amount of body energy stores. Adipokines also play key roles in triggering the physiological and metabolic dysfunction that accompanies the development of obesity. Therefore, the amount of adipose tissue accumulated during growth and development is likely to be an important factor in determining the overall health and fertility of poultry. Energy-Sensing and Metabolic Programming The ability to sense energy status and adjust metabolic pathway activity in response is a basic function of cells in all animal species [13]. En-
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is thus crucial to ensuring optimal nutrition and achieving full potential for growth and development in poultry. Control of feed intake in the short term (i.e., meal to meal) involves hormonal and neural signals originating mainly in the gut that are generated in response to the presence of feed or specific nutrients. Over the longer term, the level of body energy stored primarily in the form of lipid in adipose tissue is closely monitored. Adaptive changes in feed intake, digestion, absorption, and metabolism work together to maintain whole-body energy balance and BW in response to a constantly changing external environment. In addition to meeting immediate energy demands, feed intake can also be adjusted to ensure that energy is stored in anticipation of periods of high demand, such as egg production, or to compensate for periods of feed shortage or deprivation so as to maintain BW.
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Table 1. Peptide hormone signals associated with feed intake regulation in birds Peptide hormone
Orexigenic (stimulate)
Neuropeptide Y Agouti-related protein Peptide YY1 Pancreatic polypeptide1 Galanin Visfatin1
No effect
Melanin concentrating hormone1 Orexins (A and B)1 Motilin1
Anorexigenic (inhibit)
α-Melanocyte-stimulating hormone Cocaine- and amphetamine-regulated transcript Corticotropin-releasing factor Growth hormone-releasing hormone1 Leptin Ghrelin1 Insulin Glucagon Glucagon-like peptide 1 Cholecystokinin Bombesin Gastrin Urotensin I, urocortin Neuromedin U/S
1
Indicates a different effect in birds as compared with mammals.
ergy-sensing pathways are present in the CNS and peripheral tissues of birds, and they represent another set of regulatory mechanisms that are used to modulate peripheral tissue metabolic activity as well as regulate feed intake and energy expenditure to maintain energy balance and BW [10].
The AMP-activated protein kinase (AMPK) is a highly conserved energy sensor (an enzyme) that also regulates cellular metabolism [14, 15, and the references therein]. The AMPK is a serine-threonine kinase and a central component of a kinase signaling cascade that is a critical control point for maintaining energy homeosta-
Table 2. Potential adipokines produced by avian adipose tissue Adipokine
Proposed functions
Leptin Adiponectin Visfatin
Feed intake regulation, ovarian maturation, hepatic lipogenesis, bone remodeling Modulator of insulin sensitivity and energy homeostasis Feed intake regulation, B cell growth factor, NAD metabolism, glucose and fatty acid metabolism, insulin mimetic Resistin Innate immune response, inflammation, insulin resistance Adipsin Complement D-like molecule, serine protease Acylation-stimulating protein Fatty acid reesterification and triglyceride storage, lipolysis Adiponutrin Energy homeostasis IL-6 Acute phase inflammatory response, energy metabolism Tumor necrosis factor family (TNF-α-like1) Proinflammatory cytokine Transforming growth factor-β Regulation of cell cycle Plasminogen activator inhibitor-1 Serine protease inhibitor, blood clotting Apelin Cardiovascular function Angiotensinogen Cardiovascular function, vasoconstriction 1
Chickens do not have a TNF-α gene homolog.
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nutrient availability with tissue growth and development. Central and Peripheral Regulatory Pathways Coordinated regulation of feed intake and energy expenditure responds to external environmental cues (feed availability, feed composition, photoperiod, temperature, stressors) and internal physiological signals (hormone, nutrient, and metabolite levels). The brain, and the hypothalamus in particular, plays a pivotal role in interpreting all this information and generating the appropriate responses in feed intake and energy expenditure to maintain energy homeostasis [10]. The hypothalamic melanocortin system comprises the crucial feeding regulatory neural circuitry and is composed of 2 populations of neurons, one set that expresses neuropeptide Y (NPY) and agouti-related protein (AgRP) and a second set that expresses proopiomelanocortin (POMC), a precursor containing α-melanocyte-stimulating hormone. Stimulation of NPY/AgRP-expressing (anabolic) neurons mediates a net increase in feed intake and energy storage, whereas stimulation of the POMC-expressing (catabolic) neurons results in a net decrease in energy intake and storage. Activation of AMPK in the hypothalamus in response to lowered energy status stimulates activity of the NPY/AgRP-expressing (anabolic) neurons and thus leads to increased feed intake and reduced energy expenditure, which work together to increase energy status. Conversely, activation of mTOR causes increased activity of the POMCexpressing (catabolic) neurons, which in turn causes a reduction in feed intake and increased energy expenditure, thereby promoting the utilization of energy for maintenance, growth, and reproduction. Thus, balance in the activity of hypothalamic melanocortin system neurons is what ultimately determines whole-body energy balance and BW. Changes in the circulating levels of leptin and insulin signal the hypothalamus to bring about long-term changes in energy balance by activating or inhibiting specific hypothalamic neurons. Leptin acts on the melanocortin system within the hypothalamus, either directly or indirectly, to reduce feed intake in chickens [17]. Similarly,
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sis on both the cellular and whole-body levels. The AMPK is activated by metabolic and environmental stresses that deplete cells of energy (i.e., adenosine triphosphate). The activity of AMPK is modulated by nutrient (e.g., glucose, fatty acids) and hormonal (e.g., leptin, ghrelin, insulin, adiponectin) signals in key peripheral tissues involved in nutrient partitioning and energy metabolism (liver, skeletal muscle, and adipose tissue) as well as in neurons in specific regulatory sites within the CNS. Once activated, AMPK works to inhibit energy-consuming (anabolic) pathways such as carbohydrate, lipid, and protein synthesis while stimulating energyproducing (catabolic) pathways such as the oxidation of glucose and fatty acids. These actions are accomplished by regulating the activity and expression levels of key metabolic enzymes controlling cellular metabolism. Another important fuel-sensing kinase pathway involves the mammalian target of rapamycin (mTOR), a serine-threonine kinase complex that also responds to nutrient (e.g., amino acids) and hormonal (e.g., leptin, insulin) signaling. Like AMPK, mTOR responds to changes in energy status. However, unlike AMPK, mTOR is activated in response to elevated energy status [10]. Moreover, activation of AMPK leads to the inactivation of mTOR. In response to elevated energy status, mTOR stimulates the rate of cellular protein synthesis, growth, and proliferation commensurate with increased nutrient availability. Thus, AMPK and mTOR have overlapping but opposite functions with respect to controlling metabolic activity in response to changes in energy supply [10]. Activities of the lipid, carbohydrate, and protein metabolic pathways in the CNS and peripheral tissues are coordinately regulated by both AMPK and mTOR [10]. The AMPK controls the activity of acetyl-coenzyme A carboxylase (ACC), the rate-limiting enzyme in fatty acid biosynthesis in liver, and thus plays a key role in the modulation of lipid storage in adipose tissue [15]. The mTOR plays an important role in insulin-induced protein synthesis in skeletal muscle and is therefore an important factor in determining the growth of this tissue [16]. The combined actions of the AMPK and mTOR kinase pathways represent a regulatory mechanism linking
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THE IMPACT OF SELECTION ON FEED INTAKE REGULATION GENES Surprisingly, only a few systematic efforts have been reported that identify and characterize specific feed intake regulatory component genes in peripheral tissues and CNS in broilers as compared with other types of birds. Successful identification of such genes and the changes in their expression would provide potential genetic markers that may be useful in marker-assisted selection programs to address the problems affecting broiler breeders as well as to provide new insights into the genetic basis for regulating voluntary feed intake. In a comparison of layer and broiler chicks, Yuan et al. [19] reported that there were no differences in the expression of hypothalamic neuropeptides, including NPY, AgRP, POMC, and orexin, between the 2 groups at 7 d posthatch, despite the fact that BW and feed intake were already markedly different at this age. Similarly, the expression of associated genes such leptin receptor, ACC, and fatty acid synthase was also similar between the 2 groups in the hypothalamus. However, broiler chicks expressed higher levels of the glucocorticoid receptor in the hypothalamus, which was associated with lower levels of corticotrophin-releasing hormone expression. This could account for increased feed
intake in broilers. They also found higher expression of the fat mass and obesity-associated gene in broiler chicks as compared with layer chicks. The latter findings provide possible candidate marker genes, although that remains to be confirmed and validated. Byerly et al. [20] used cDNA microarrays and individual gene expression analysis to assess differential expression of anabolic/orexigenic and catabolic/anorexigenic genes in hypothalamic samples from fat and lean selected chicken lines. They reported that interactions between the neuropeptide brainderived neurotrophic factor and the hormones T3 and corticosterone might constitute a mechanism linking hypothalamic energy regulation with body composition by controlling expression of specific CNS obesity network genes, including leptin receptor, POMC, NPY, AgRP, and thyroid-releasing hormone. Ka et al. [21] compared 2 populations of chickens selected for BW at 56 d of age (selected for high and low weight) using cDNA microarray technology to determine differences in gene expression in a portion of the brain (diencephalon) containing the major metabolic regulatory regions, including the hypothalamus and brain stem. No definitive changes in expression of major regulatory components (i.e., neuropeptides and receptors) were detected and only small changes were found in genes thought to regulate neuronal plasticity and lipid metabolism. Thus, no specific candidate genes were identified, suggesting that the extreme differences in BW phenotypes were the net result of small contributions from multiple genes. The authors further suggested that selection over many generations for increased juvenile BW in chickens had caused CNS function to adapt at different rates posthatch in the 2 groups, and this may account for the observed differences in feeding behavior. There has been some investigation using transcriptional profiling of liver tissue from lean vs. fat and fast- vs. slow-growing selected lines of broiler chickens to identify differentially expressed genes [22, 23]. Generally, these studies highlighted differences in metabolic enzymes and transcription factors, suggesting those genes as possible candidates for further study. These findings emphasize the importance of coordinately regulated metabolic pathways, such as
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insulin administered directly into the brain inhibits feed intake in chickens, and the anorexia produced in response to insulin signaling is associated with increased expression of POMC, cocaine- and amphetamine-regulated transcript, and corticotrophin-releasing hormone genes in the hypothalamus [18]. These effects may also involve an insulin-mediated increase in hypothalamic mTOR activity. Because plasma levels of both leptin and insulin rise and fall with increases and decreases in energy status, such as during fasting and refeeding in broilers, it is possible that these 2 key metabolic hormones could serve as peripheral signals of energy storage to the CNS in birds [10]. In doing so, they would be expected to play an important role in modulating hypothalamic melanocortin neural activity to produce appropriate changes in feed intake and energy expenditure to achieve energy homeostasis.
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FEED RESTRICTION IN FEMALE BROILER BREEDER MANAGEMENT The central difficulty associated with the management of modern female broiler breeder strains involves the inability of these birds to adequately self-regulate feed intake during growth and development to achieve an optimal BW and composition needed to support efficient egg and chick production by the hen. Therefore, female breeders are subjected to a high degree of feed restriction early in life. It has been suggested that the 7- to 15-wk period of the pullet growth phase is the most critical period for limiting BW increase and thus represents the phase of production requiring the highest degree of feed restriction [26]. In fact, during the rearing phase, feed allocation can be reduced by as much as one-third of the intake of ad libitum-fed birds of the same age or approximately one-half that of birds at the same BW [27]. To achieve better flock uniformity in commercial breeder produc-
tion, skip-a-day (SKP), 5–2, or 4–3 programs are often used in preference to providing a restricted amount of feed on an every-day (ED) basis [28]. Because of the severity of feed restriction imposed during the pullet phase of production, concerns continue to be raised about the effects on bird welfare [1]. However, the benefits of feed restriction to performance of the breeder hen are well known and include reduced BW, delayed sexual maturity, improved ovarian function with fewer multiple ovulations, higher egg production with better persistence and longer sequences, reduced numbers of abnormal eggs, and lower mortality during the laying period [1]. These observations support the need for feed restriction in the management of the broiler breeder because they demonstrate clear production benefits that outweigh the health problems associated with the development of obesity in unrestricted birds. Attempts to moderate or alleviate the need for feed restriction through the use of diet dilution (i.e., qualitative restriction) or the introduction of alternative genotypes, such as those containing the dwarf gene, have produced mixed results with respect to maintaining female breeder production efficiency [3]. Thus, a nonrestrictive feed management solution that balances production and welfare concerns does not appear to be a realistic possibility [1]. Because primary breeders maintain the selection pressure for increased juvenile growth rate and efficiency in subsequent generations of broilers, the divergence between broiler and broiler breeder BW targets continues to widen. As a result, the intensity of feed restriction will continue to increase to sustain adequate reproductive efficiency in the breeder female [4]. To date, there have been only a few reports concerning the physiological and metabolic consequences of restricted feeding in the female broiler breeder. In light of the previous discussion of energy signaling and sensing mechanisms used to regulate feed intake in birds, it is important to determine the impact of feed restriction on innate regulatory mechanisms to better assess the implications for overall health and well-being of the managed bird. The following brief discussion focuses on what is currently known about the impact of feed restriction regimens currently in use on hormonal and metabolic profiles in the female breeder.
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the lipogenic pathway in liver, as critical control points for maintaining whole-body energy balance. More studies are required to fully understand the genetic changes related to the control of feed intake and energy expenditure that have accompanied intensive selection of the modern broiler. One likely comparison that has not yet been undertaken, but that would provide highly relevant information, is to compare randombred (unselected) broiler strains with modern highly selected ones. Such a comparison was performed by Havenstein et al. [24] to demonstrate a 4.6fold increase in growth rate between 1957 and 2001. Moreover, they reported that only 10 to 15% of the 6-fold improvement in carcass yield was accounted for by nutritional changes, with 85 to 90% of the increase attributable to genetics [25]. The application of new functional genomic techniques to analyze key tissues (brain, liver, skeletal muscle, gut, adipose tissue) from such populations would yield highly useful information concerning what has changed in response to selection for growth and meat yield in the modern broiler. This is especially relevant for the genes involved in feed intake and energy homeostatic regulatory mechanisms. Clearly, this is an area that merits further study.
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ED feed allocation regimen with some degree of relaxation of the restriction. Whether the differences between ED and SKP feeding during the rearing period continue to affect birds after sexual maturity is unclear but merits further investigation. Without any feed restriction from hatch, breeder females can achieve a BW more than twice that of restricted-fed birds at the time of photostimulation, with double the amount of carcass fat at peak egg production [31, 32]. Because voluntary feed intake naturally declines and approaches ad libitum levels after BW reaches a plateau [31], ad libitum feeding before photostimulation has been evaluated as a means to allow for enhanced nutrition to meet the needs for egg production and to relax the feed restriction. However, a rapid rate of BW gain at sexual maturity has also been shown to decrease egg production [1]. Figure 1 shows the concentrations of 4 major metabolic hormones (insulin, leptin, T3, and IGF-I) in plasma from breeder females switched to ad libitum feeding at 21 wk of age (1 wk before photostimulation) or maintained on an ED feeding regimen through the plateau period of egg production. The levels of insulin and leptin were elevated in the birds fed ad libitum, especially before and just after photostimulation at 22 wk in the critical period leading to sexual maturity (i.e., first egg) [33, 34]. Changes in circulating hormones such as insulin and leptin signal the status of energy storage (i.e., abdominal fat pad size) and, in conjunction with T3, they also help regulate hepatic metabolic programs such as lipogenesis, which is a key determinant of energy storage in the bird. The ad libitum-fed breeders demonstrated increased hepatic expression of the ACC gene, which persisted throughout egg production (Figure 2). Similar findings were also noted for the expression of other lipogenic genes in the liver of ad libitum vs. restricted birds [33]. Changes in hepatic lipogenic enzyme gene expression were accompanied by increases in fat pad size and ovary weight compared with restricted-fed birds (Figure 2). These processes are linked and coordinately regulated in the breeder hen. Reduced total egg production and an increased number of abnormal eggs in response to ad libitum feeding were observed [33]. Together these
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There have been 2 recent reports comparing the effects of commonly used feed-restriction regimens during the rearing phase, ED vs. SKP, on plasma hormones and metabolites and on hepatic lipid metabolism in pullets at 16 wk of age [29, 30]. Periods without feed in the SKP birds resulted in a variety of changes in the plasma hormone and metabolite profiles. These changes included increased thyroxine, corticosterone, and glucagon. Plasma free fatty acid (nonesterified free fatty acid) levels increased during fasting (period without feed) as a result of lipid mobilization to provide energy, and lipid mobilization was likely stimulated by the increase in glucagon. Plasma insulin, T3, IGF-I, and triglyceride levels were reduced in SKP compared with ED birds, whereas plasma IGF-II levels appeared less responsive to feed deprivation. In general, the 2 feeding regimens produced marked changes in endocrine and metabolite profiles despite the fact that an identical amount of feed was consumed over time by both groups. The differential effects on metabolism were most likely the result of the unique changes in hormonal signaling that accompanied the 2 restriction regimens. Skipping 24-h periods of feeding, as is practiced in SKP, 5–2, or 4–3 programs, is believed to set up a state of repeated fasting-refeeding cycles [27]. Such a condition is thought to affect overall metabolic efficiency because of the constant need to store and release greater quantities of nutrients than if they were provided on a regular (ED) basis. Because the storage and mobilization of nutrients is not a totally efficient process, such nutrient turnover likely accounts for the reduced efficiency of the SKP vs. ED birds [27]. The findings that SKP caused more dramatic increases in the expression of the liver lipogenic genes ACC, fatty acid synthase, and malic enzyme compared with ED reflects a greater fluctuation in nutrient and energy supply caused by the recurring 24-h periods without feed [29]. The benefits of improved flock uniformity associated with SKP programs must be carefully weighed against the potential savings in feed cost and possible improvements in performance and efficiency attainable by using ED programs [27]. At or just before sexual maturity, most broiler breeders are typically switched to an
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Figure 1. Plasma levels of the major metabolic hormones insulin, leptin, triiodothyronine (T3), and insulin-like growth factor-I (IGF-I) in female broiler breeders fed ad libitum (Ad Lib) or maintained in feed restriction from 21 wk of age (Restricted). Plasma samples were collected before photostimulation (prelight, 22 wk), after photostimulation (postlight, 24.5 wk), at first egg, and at the plateau of egg production (36.5 wk). All values represent the mean ± SEM of 21 (pre- and postlight) or 40 (first egg and plateau) analyses. Different letters (a–f) designate significant differences (P < 0.05). Data depicted are from Sun et al. [34].
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findings emphasize the benefits of maintaining feed restriction (i.e., ED regimen) throughout the egg-laying period. Previously, it was shown that the multiple hierarchies and erratic ovulation that accompany ad libitum feeding of breeders are associated with abnormal regulation of follicle maturation and steroidogenesis in the ovary [1]. It is possible that increased circulating leptin levels observed in ad libitum-fed breeders affected ovarian follicular maturation because the levels of leptin receptor are upregulated in these birds during maturation of large yellow follicles [35]. Furthermore, administration of leptin to laying hens is known to advance sexual maturation by increasing follicular development and reducing apoptosis [36]. Therefore, it is possible that leptin could play a significant role in ovarian dysfunction in ad libitum-fed breeder hens [35]. However, an association between abdominal fat pad size (i.e., source of leptin) and the potential effects of leptin on ovarian function remains to be shown in birds. Moreover, defining a role for leptin in ovarian function is complicated by the controversy over the existence of the avian leptin gene [10]. Solving the controversy surrounding
this hormone will greatly aid our understanding of the potential role(s), if any, of leptin in avian biology. Changes in plasma IGF-I observed between restricted and ad libitum-fed breeders (Figure 1) could also have potential effects on the ovary because this growth factor is known to play an important localized role in ovarian function [37]. In summary, different feeding regimens used during the rearing and egg-laying phases of production have important effects on hormonal levels and key metabolic pathways in the female broiler breeder. Understanding the links between feed management and the consequent effects on hormones and metabolism will aid producers in meeting the nutritional requirements of birds at different phases of production through better feed management practices.
CONCLUSIONS AND APPLICATIONS
1. Feed restriction has now become an important and indispensable management tool for female broiler breeder production. How feed allocation is managed can have a significant impact on female
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Figure 2. Analysis of mRNA expression for the acetyl-coenzyme A carboxylase (ACC) gene in liver from female broiler breeders fed ad libitum (Ad Lib) or maintained in feed restriction from 21 wk of age (Restricted). Also shown are the corresponding relative abdominal fat pad and ovary weights. Values represent the mean ± SEM of 5 determinations for ACC gene expression and 21 (pre- and postlight) or 40 (first egg and plateau) for liver and ovary weight analyses. Different letters (a–d) designate significant differences (P < 0.05). Data depicted are from Richards et al. [33] and Sun et al. [34].
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