Welfare and breeding in broilers

A concern over how to feed the rising human population while at the same time minimizing the effect on the environment has led to calls for agriculture to become more ‘sustainably intensive’ and more efficient. (Royal Society, 2009; Steinfeld et al., 2006; Garnett et al., 2013; Gerber et al., 2013). The human population is projected to be at least 9 billion by 2050 (FAOStat, 2009; Godfray et al., 2010) and the current trend is for the consumption of meat and dairy products to keep on rising (Gerber et al., 2013) as people become wealthier and want what they see as a better diet. Chickens are already, at 58 billion killed each year, the most commonly consumed animal (FAOStat, 2012) and projected to overtake pork by tonnage as well as numbers by 2020, with most of the increase is expected to occur in SE Asia and sub-Saharan Africa (USDA, 2013; Gerber et al., 2013).

Modern breeds of broilers are already highly efficient producers of protein due to a combination of diet, management and, in particular, selective breeding for high juvenile growth rate, breast meat yield and efficiency of food conversion (Flock et al., 2005; Bessei, 2006; Estevez, 2007; Arnould and Leterrier, 2007). However, this selective breeding has had side-effects on the health and welfare of the birds including susceptibility to cardiovascular disease (Julian, 1995; Mitchell, 1997) and lameness (Kestin et al., 1992; Rauw et al., 1998; Sanotra et al., 2001; Bradshaw et al., 2002; Burt, 2002; Knowles et al., 2008). Selective breeding for fast juvenile growth rate has also had knock-on effects on the welfare of the parent birds (‘breeders’). Without feed restriction, these breeder birds rapidly become obese (Dunnington and Siegel, 1985), have locomotory problems (Katanbaf et al., 1989), the males have reduced fertility (McGary et al., 2002). While these negative symptoms can be avoided by restricting the amount of food that the growing breeders receive, this is often only 25-50% of what the birds would consume if fed ad libitum (Savory et al., 1993; Ducuypere et al., 2007; Renema et al., 2007) and raises welfare problems of its own since birds exhibit signs of chronic or metabolic hunger (Mench, 2002; de Jong et al., 2002; Hocking, 2004; D’Eath et al., 2009). Furthermore, as broiler growth has continued to increase, the degree of feed restriction needed to keep broiler breeders on a healthy growth trajectory has also increased (Renema et al., 2007).

These findings raise serious questions about what will happen to the welfare of chickens in the future. If breeding for greater ‘efficiency’ in broiler production over the last 50 years has already resulted in welfare problems in both broilers and breeders, what will happen to bird welfare in the face of calls for even higher efficiency and better feed conversion (Lawrence, 2008; Dawkins, 2012)? Will breeding for greater efficiency inevitably mean compromising animal welfare? Are there limits as to how far we can push selective breeding before socially unacceptable limits to welfare are reached (Sandøe et al., 2009)?

The key question I want to address is in fact not ‘ Is there a conflict between breeding for welfare and breeding for production?’ because that refers to the current situation, with our current breeds and our current knowledge about chicken genetics and we should not underestimate our ignorance about genetics. Despite having sequenced the genomes of many different species including the chicken (ICGSC, 2004) there is still much we do not know about how genes actually work to build bodies and how they interact with each other (Jensen and Andersson, 2005) so that we cannot predict what might be achieved or what might or might not be possible. For this reason, the question I want to address instead is ‘Looking to the future, is a conflict between breeding for production and breeding for welfare inevitable?’ In other words, will breeding for the improved production traits demanded by the more efficient, more environmentally sensitive agriculture of the future mean that there will be an inevitable decline in animal welfare? Or, might there be ways in which the right breeding programmes for greater efficiency might actually protect or even improve animal welfare? (Jones & Hocking 1999; Arnould and Leterrier 2007; Thiruvenkdan et al., 2011; Dawkins and Layton, 2012). Although it is impossible to be certain of the answers, there are some pointers that could be useful guides to the future. Some are warnings and some are as yet untapped opportunities. 

Albers (1998) argued that the genetic limits to broiler breeding would be reached in 20 years time, now only 4 years away. In wild animals, there is evidence of constraints and limits on what natural selection can achieve in that over 99% of all the species that have ever existed on Earth are now extinct (Simpson, 1983). Some of these extinctions occurred because particular lines evolved into new species better adapted to changing conditions than their ancestors, so these lines did not die out altogether. For example, at least one dinosaur lineage did not die out: it evolved into birds and still lives today. But many extinctions have involved the complete elimination of major groups, such as the trilobites, which suggests that such lineages were limited in the extent to which they could change in the face of a changing environment or at least in how fast they could change. The limits on natural selection include pleiotropy (genes with both desirable and undesirable effects), historical constraints (such as the blind spot in the vertebrate eye) and the simultaneous evolution of other organisms, such as predators and diseases, engaged in a constant arms race to run faster or to overcome immune resistance (R. Dawkins, 1982).

Many of these same constraints and limits also exist for artificial breeding programmes, although artificial selection has the advantage over natural selection that some of these constraints can be relaxed (D’Eath et al., 2010). It is possible to import new genetics, for example, and to greatly increase the range of mutants that selection has to work on. We can keep animals alive that would die in nature (such as ones that need our help in mating) and there is also a sense that we are beginning to literally go back to the drawing board and ‘design’ animals for the goals we want. We can hope to produce animals with traits and combinations of traits that could in the end be successful and have high welfare, but which would never have been possible in the wild. However, that does not mean that we will not reach ultimate limits on what can be achieved. We need to bear in mind that both natural selection and artificial selection may have limits and that animals are not infinitely malleable. Furthermore, we may also reach ethical limits of what society will tolerate even if genetics would allow further change (Sandøe et al., 2009). Even if it remains economic to breed ever more efficient broilers, but at a cost of seriously impaired welfare, people might find this so unacceptable that they would stop buying chicken. It has therefore been argued that sustainable breeding programmes must contain safeguards against a decline in welfare standards (Jensen and Andersson, 2005; Sandøe et al., 2009). But genetics can do more than simply halting a decline in welfare. Selection for traits such as increased disease resistance, leg strength and liveability can actually improve it (Jones & Hocking 1999; Arnould and Leterrier 2007; Aggrey, 2010; Thiruvenkdan et al., 2011). Whether this will actually happen in practice depends on whether breeding broiler chickens for better welfare necessarily means reversing the production and efficiency gains that have been achieved over the last 60 years. Are there ways in which better welfare could be incorporated into breeding programmes that would be compatible with, or even enhance efficiency and so be more likely to be adopted? 

A simple definition of good welfare is that animals are healthy and have what they want (Dawkins, 2008). Sometimes, breeding for better welfare will have clear and direct commercial benefits to producers. Healthy, high welfare animals bring a range of commercial benefits such as lowered mortality, reduced food waster, higher quality products, lower costs of medication, and public approval leading to a willingness of consumers to pay more for high welfare food.

Sometimes, on the other hand, welfare and efficient production appear to be in direct conflict. Breeding programmes based on economically important production traits have been directly linked to reduced welfare (Rauw, et al., 1998; Jones and Hocking, 1999; Sandoe, et al., 1999; Renema et al., 2007). However, this is not because reduced welfare is always a consequence of selective breeding but rather, because until recently, the breeding goals have been set too narrowly with concentration on one or a few production traits (Simm, 1998; Rauw et al., 1998). By broadening the selection criteria it may be possible to reduce the apparent conflict and achieve a wider range of goals (Lawrence et al., 2004; Beaumont and Chapuis, 2004; D’Eath et al., 2010; Dawkins and Layton, 2012). 

Breeding companies now increasingly incorporate health and welfare goals alongside economic ones into their breeding programmes and use a variety of traits such as leg health and feather cover, as well as meat yield and feed conversion efficiency to select their breeding birds (Katanbaf and Hardiman, 2010). However, from a welfare point of view, growth rate is still seen as the problem (Cooper and Wrathhall, 2010), leading to an apparent direct conflict between selecting for good welfare and selecting for production. But is this conflict inevitable or might it be possible to genetically select birds that had both high growth rate and high welfare? The key question here is whether the current observed correlations between growth rate and welfare problems arise because these traits are inextricably linked or whether, with different breeding strategies, they could be separated. Here we can learn some lessons from evolution and what happens under natural selection.

In wild animals, there are many examples of high juvenile growth rate with no ill effects. In fact, in many species of birds with short breeding seasons or a high risk of predation, natural selection has favoured young birds that grow as rapidly as possible out of their most vulnerable stage (Remes and Martin, 2002). Birds that breed in the arctic, such as the Red Knot (Calidris canutus) and Greater Snow Goose (Chen caerulescens atlantica), have adapted to the short summers by having chicks that grow much faster and are independent of their parents earlier than their temperate counterparts (Fortin et al., 2000; Schekkerman et al., 2003). Juvenile growth can speed up under the influence of natural selection to yield healthy juveniles and adults (Arendt, 1997), so that there is nothing intrinsically wrong with a high juvenile growth rate. What matters is that the juvenile body also evolves so that it can deal with the rapidly increasing weight. The problem is not the high growth rate itself but the way that growth rate is achieved.

In nature, a fast-growing young animal whose skeleton could not support its body weight would die. Fast juvenile growth will only be favoured if there are also changes in the skeletal, muscle and other systems of the body so that the fast growth is also healthy growth. Natural selection is almost always multi-trait selection – that is, selection is not just for one trait at a time, but fine tuning of the whole body with changes occurring in many different genes to accommodate the increased growth rate. By contrast, many breeding programmes have concentrated on just a small number of traits, usually to do with growth rate and other production outcomes. Fast growth rate may not in itself be a problem, but it can easily become so if the breeding programme is focussed on a small number of traits rather than selecting for a wide variety of health and welfare traits alongside production ones. The solution is to learn from evolution by natural selection and to develop multi-trait breeding programmes that select for a wider range of goals (Lawrence et al., 2004; Beaumont and Chapuis, 2004). This may mean not just ensuring ‘no decline in welfare’ but positive selection for good welfare, so that good health, liveability, walking and disease resistance are given even higher priority and consequently improve. 

Another potential conflict between production and welfare occurs between selecting for commercial productivity of broilers and the concomitant need to restrict-feed the parent birds need to maintain their health. ). The ‘breeder dilemma’ (Decuypere et al., 2006; Kasanen et al., 2010) is that there are welfare issues of health if feed restriction is not imposed and there are welfare issues of hunger if it is not.

Barbato (1991) suggested that a way forward would be to select birds at different stages of their growth. Breeding programmes that altered the shape of the broiler growth curve could maintain the necessary early growth and protein accretion in the young birds while curbing later growth and fat deposition in the adults. Instead of seeing body weight at a given age as the result of a single function ‘growth rate’, it should be seen as the result of at least two separate growth phases (Grossman and Koops, 1988).

This is fully in line with what happens in wild animals where different selective pressures operate at different stages of the life cycle and growth rates of embryos, juveniles and adults vary independently (Ricklefs, 2010). The juvenile is not an inadequate stage on the path to adulthood but has to be fully functional in its own right. Each species has its own growth trajectory that is achieved by having different genes coming into play at different stages of life (Zera and Harshman, 2001).

Divergent selection of broilers for growth rate at 14 days of age and separately for percentage body fat at 42 days has shown that that early growth in juveniles can indeed be genetically uncoupled from adult obesity, resulting in birds that have early high growth but lack the high percent of body fat typical of obese adults (Sizemore and Barbato, 2002; Kerr et al., 2001). More recent QTL analysis has now shown that there are different sets of genes controlling growth at different stages of the life cycle (Gao et al., 2010; Ankra-Badu et al., 2010), giving a genetic underpinning to multi-age selection.

Both multi-trait and multi-age selection are thus important ways of resolving apparent conflicts between breeding goals. The idea that breeding for high welfare in broilers and breeders inevitably involves selecting for slower juvenile growth rate and is on a collision course with efficient production, therefore needs to be challenged by breeding programmes with a wider range of strategies than have been adopted up to now.

The breeding programmes could also benefit from looking outside modern commercial lines to increase the range of genotypes that can be selected. This is a particularly important consideration for broiler chickens because of the possibility that many generations of selection for a narrow range of traits may have eliminated the variation necessary for breeding for a broader range. Indeed, the genetic diversity present in modern commercial pure lines has been estimated to be only 50% of that present in ancestral breeds (Muira et al., 2008). On the other hand, comparisons of single-nucleotide polymorphisms (SNPs) between junglefowl and domestic lines have not supported the idea of reduced variation among domestic breeds taken as a group. On the contrary, most of the SNPs (Single Nucleotide Polymorphisms) identified in junglefowl also appear to be present in broilers, suggesting that they originated before domestication (Wong et al., 2004). Artificial selection on broilers has also lead to an increase in the recombination rate (Groenen et al., 2009), giving a persistent wide range of variation in each generation.

There is thus evidence of a great deal of useable variation still existing within modern breeds of chickens (Hill, 2010), but it order to maximize the potential of any multi-trait breeding programme for broilers, it may be valuable to utlilise as many different sources of genetic variation as possible, such as using a wide range of breeds from different parts of the world to reintroduce “missing alleles” that may have been lost in the course of domestication or more recent selection for particular traits. These include the ‘Three Yellow’ from China and other varieties of chickens native to particular areas (Yang and Jiang, 2005) and ‘high welfare’ breeds such as those used in Label Rouge production (N’Dri et al., 2007; Lariviere and Leroy, 2010).

The search for multi trait birds could also be enhanced by introducing specific genes to commercial breeds, using modern genetic techniques that can identify and target genes more precisely (Sandøe, 2010; Lyell et al., 2011). 

For thousands of years, humans have altered the shape and behaviour of domesticated animals by breeding from animals that had characteristics they regarded as desirable, but without any knowledge of the underlying genetic mechanisms. This proved remarkably successful, giving us breeds of dogs, chickens, cattle, pigs and sheep suited for different purposes and well adapted to the environments in which they lived

The twentieth century saw the rise of the science of genetics and with it came more control over animal breeding through more active decisions over which animals mated with each other ones. Measurements of heritability and the correlations between traits allowed the choice of animals for breeding to be made not just on the phenotypic qualities of the animal itself but of those of its offspring and other relatives (Simm, 1998). Furthermore, it is now realized that because of genotype x environment interactions, these phenotypic qualities need to be measured in the environment in which they are to be used. For example, measuring FCR (food conversion ratio) in Label Rouge chickens kept in cages (to facilitate the measurement of how much each bird eats and its daily weight gain) does not give a good indication of FCR when the birds are kept on free range outside (N’Dri et al., 2007). Any breeding programme designed to improve the welfare of broilers thus needs to select animals in situ – in the environment for which they are intended, particularly for disease resistance and for behavioural and social traits (D’Eath et al., 2010; Rodenberg et al., 2010).

The twenty-first century brings even greater opportunities for controlling breeding programmes in poultry (Muira et al., 2008; Rothschild and Plastow, 2008), beginning with the sequencing of the chicken genome in 2004 (ICGSC, 2004). Now we have a range of techniques that enable us to map genetic pathways that control growth, development and metabolism of chickens (Cogburn et al., 2003) and can even reveal which genes are active at particular points in development (Cogburn et al., 2003). Marker assisted selection using QTLs (Quantitative Trait Loci) enables more efficient identification of birds with desirable traits and so speeds up the process of selection, but this very efficiency brings with it dangers and ethical issues (D’Eath et al., 2010). The research emphasis so far has been on broiler traits associated with production such as growth rate (Wahlberg, et al., 2009; Nie et al., 2010), feed conversion (Pakdel et al., 2005; Gonzales-Recio et al., 2009) carcass quality (Zhang et al., 2009) and egg production (Zhang et al., 2008). While some attention has been paid to traits associated with welfare (Keeling et al., 2004), there is a danger of once again focussing too narrowly on commercially valuable traits and neglecting the importance of selecting for many traits including welfare (Lawrence et al., 2004) simply because less is known about them. The side-effects of using modern techniques to apply even more intense selection than is possible with conventional breeding are unknown (D’Eath et al., 2010). Even if chicken genotypes are selected with sophisticated new techniques, the resulting phenotypes are still going to have to be scrutinized for welfare in the real world. Until we have a much greater knowledge than we do at present of all the main effects and side effects (pleiotropisms, linkages etc) of the genes that are being manipulated, we will not do away with the need for classical genetics or even traditional methods for selecting animals. On the contrary, achieving the multiple goals for broilers will need assessment of the phenotype in the environment in which it will be reared and at many different stages of its life even more urgently than ever. 

A combination of genetics and ethics raises difficult issues about acceptable standards of welfare and commercial production of chickens and whether efficiently produced, healthy, high welfare, environmentally friendly chicken meat is possible. I have argued that we currently do not yet have the scientific knowledge we need to resolve these issues. Before assuming that welfare and efficiency are inevitably in conflict, we need to challenge widely held assumptions, such as that commercially valuable growth rate is inevitably linked to poor welfare or that high juvenile growth rate will always result in the need to restrict feed the parents. These challenges should come in the form of breeding programmes whose aims are to improve both welfare and efficiency. Only by breeding positively for better welfare will be know whether apparent conflicts between welfare and production are real and inevitable or whether they are simply the result of breeding programmes of the past having had too narrow a range of breeding goals.

Broiler chicken welfare is most likely to be improved in practice if animal welfare traits such as good walking ability, good feathering and healthy legs and feet are seen as compatible, rather than in conflict, with other goals such as commercial production. This suggests that breeding programmes that prioritize high welfare as a major breeding goal may be able to satisfy commercial needs alongside welfare and other important goals. 

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