The Science of Animal Suffering

Can suffering in non‐human animals be studied scientifically? Apart from verbal reports of subjective feelings, which are uniquely human, I argue that it is possible to study the negative emotions we refer to as suffering by the same methods we use in ourselves. In particular, by asking animals what they find positively and negatively reinforcing (what they want and do not want), we can define positive and negative emotional states. Such emotional states may or may not be accompanied by subjective feelings but fortunately it is not necessary to solve the problem of consciousness to construct a scientific study of suffering and welfare. Improvements in animal welfare can be based on the answers to two questions: Q1: Will it improve animal health? and Q2: Will it give the animals something they want? This apparently simple formulation has the advantage of capturing what most people mean by ‘improving welfare’ and so halting a potentially dangerous split between scientific and non‐scientific definitions of welfare. It can also be used to validate other controversial approaches to welfare such as naturalness, stereotypies, physiological and biochemical measures. Health and what animals want are thus not just two of many measures of welfare. They provide the definition of welfare against which others can be validated. They also tell us what research we have to do and how we can judge whether welfare of animals has been genuinely improved. What is important, however, is for this research to be done in situ so that it is directly applicable to the real world of farming, the sea or an animal’s wild habitat. It is here that ethology can make major contributions.     

Role of very slightly deleterious mutations in molecular evolution and polymorphism

Several models of multiple slightly deleterious alleles are reviewed and theoretical consequences of slightly negative selection are discussed in conjunction with evolution and variation at the molecular level. Facts are organized which may be satisfactorily explained by the hypothesis of very slightly deleterious mutations. They are: (1) There appears to be an upper limit in heterozygosity for protein loci as measured by electrophoresis. (2) The excess of rare alleles is more pronounced in Drosophila than in man. (3) Correlation of heterozygosities at a locus among sibling species of the Drosophila willistoni group is too high compared to what is expected by the strict neutral theory, while it is not so among human races and between man and chimpanzee. (4) The rate of protein divergence is exceptionally high in Hawaiian Drosophila.     

Recent admixture generates heterozygosity–fitness correlations during the range expansion of an invading species

Admixture, the mixing of historically isolated gene pools, can have immediate consequences for the genetic architecture of fitness traits. Admixture may be especially important for newly colonized populations, such as during range expansion and species invasions, by generating heterozygosity that can boost fitness through heterosis. Despite widespread evidence for admixture during species invasions, few studies have examined the demographic history leading to admixture, how admixture affects the heterozygosity and fitness of invasive genotypes, and whether such fitness effects are maintained through time. We address these questions using the invasive plant Silene vulgaris, which shows evidence of admixture in both its native Europe and in North America where it has invaded. Using multilocus genotype data in conjunction with approximate Bayesian computation analysis of demographic history, we showed that admixture during the invasion of North America was independent from and much younger than admixture in the native range of Europe. We tested for fitness consequences of admixture in each range and detected a significant positive heterozygosity–fitness correlation (HFC) in North America; in contrast, no HFC was present in Europe. The lack of HFC in Europe may reflect the longer time since admixture in the native range, dissipating associations between heterozygosity at markers and fitness loci. Our results support a key short‐term role for admixture during the early stages of invasion by generating HFCs that carry populations past the threat of extinction from inbreeding and demographic stochasticity.     

The strength of the association between heterozygosity and probability of interannual local recruitment increases with environmental harshness in blue tits

The extent of inbreeding depression and the magnitude of heterozygosity–fitness correlations (HFC) have been suggested to depend on the environmental context in which they are assayed, but little evidence is available for wild populations. We combine extensive molecular and capture–mark–recapture data from a blue tit (Cyanistes caeruleus) population to (1) analyze the relationship between heterozygosity and probability of interannual adult local recruitment and (2) test whether environmental stress imposed by physiologically suboptimal temperatures and rainfall influence the magnitude of HFC. To address these questions, we used two different arrays of microsatellite markers: 14 loci classified as neutral and 12 loci classified as putatively functional. We found significant relationships between heterozygosity and probability of interannual local recruitment that were most likely explained by variation in genomewide heterozygosity. The strength of the association between heterozygosity and probability of interannual local recruitment was positively associated with annual accumulated precipitation. Annual mean heterozygosity increased over time, which may have resulted from an overall positive selection on heterozygosity over the course of the study period. Finally, neutral and putatively functional loci showed similar trends, but the former had stronger effect sizes and seemed to better reflect genomewide heterozygosity. Overall, our results show that HFC can be context dependent, emphasizing the need to consider the role of environmental heterogeneity as a key factor when exploring the consequences of individual genetic diversity on fitness in natural populations.     

Specific alleles at immune genes,rather than genome‐wide heterozygosity,are related to immunity and survival in the critically endangered Attwater's prairie‐chicken

The negative effects of inbreeding on fitness are serious concerns for populations of endangered species. Reduced fitness has been associated with lower genome‐wide heterozygosity and immune gene diversity in the wild; however, it is rare that both types of genetic measures are included in the same study. Thus, it is often unclear whether the variation in fitness is due to the general effects of inbreeding, immunity‐related genes or both. Here, we tested whether genome‐wide heterozygosity (20 990 SNPs) and diversity at nine immune genes were better predictors of two measures of fitness (immune response and survival) in the endangered Attwater's prairie‐chicken (Tympanuchus cupido attwateri). We found that postrelease survival of captive‐bred birds was related to alleles of the innate (Toll‐like receptors, TLRs) and adaptive (major histocompatibility complex, MHC) immune systems, but not to genome‐wide heterozygosity. Likewise, we found that the immune response at the time of release was related to TLR and MHC alleles, and not to genome‐wide heterozygosity. Overall, this study demonstrates that immune genes may serve as important genetic markers when monitoring fitness in inbred populations and that in some populations specific functional genes may be better predictors of fitness than genome‐wide heterozygosity.     

Identification of Microsatellite Repeats in Turbot (Scophthalmus maximus) and Dover Sole (Solea solea) using a RAPD-Based Technique: Characterization of Microsatellite Markers in Dover Sole

We have used a RAPD-based technique to identify several microsatellite repeats in turbot (Scophthalmus maximus) and Dover sole (Solea solea) and report the characterization of six novel polymorphic microsatellite markers for Dover sole. These are the first such markers to be developed for this flatfish species. They exhibit much higher levels of heterozygosity than those previously observed with allozyme loci and should prove useful in addressing population genetic questions as well as more fundamental aquaculture-related questions. Received ; accepted July 13, 1999.     

On the lack of evidence that non-human animals possess anything remotely resembling a 'theory of mind'

After decades of effort by some of our brightest human and non-human minds, there is still little consensus on whether or not non-human animals understand anything about the unobservable mental states of other animals or even what it would mean for a non-verbal animal to understand the concept of a ‘mental state’. In the present paper, we confront four related and contentious questions head-on: (i) What exactly would it mean for a non-verbal organism to have an ‘understanding’ or a ‘representation’ of another animal''s mental state? (ii) What should (and should not) count as compelling empirical evidence that a non-verbal cognitive agent has a system for understanding or forming representations about mental states in a functionally adaptive manner? (iii) Why have the kind of experimental protocols that are currently in vogue failed to produce compelling evidence that non-human animals possess anything even remotely resembling a theory of mind? (iv) What kind of experiments could, at least in principle, provide compelling evidence for such a system in a non-verbal organism?     

Behaviour as a tool in the assessment of animal welfare

A central issue in animal welfare research is how to assess the welfare state of animals objectively and scientifically. I argue that this issue can be approached by asking two key questions: 1) is the animal physically healthy and 2) does the animal have what it wants? Behaviour is used to answer both of these questions. In the assessment of physical health, it can be used for clinical and pre-clinical diagnosis. In the assessment of what animals want, it has a major role through choice and preference testing. It is particularly important that applied ethologists develop methods for assessing welfare in situ--in the places where concern for animal welfare is greatest such as on farms and in zoos.     

Heterozygosity at a single locus explains a large proportion of variation in two fitness‐related traits in great tits: a general or a local effect?

In natural populations, mating between relatives can have important fitness consequences due to the negative effects of reduced heterozygosity. Parental level of inbreeding or heterozygosity has been also found to influence the performance of offspring, via direct and indirect parental effects that are independent of the progeny own level of genetic diversity. In this study, we first analysed the effects of parental heterozygosity and relatedness (i.e. an estimate of offspring genetic diversity) on four traits related to offspring viability in great tits (Parus major) using 15 microsatellite markers. Second, we tested whether significant heterozygosity–fitness correlations (HFCs) were due to ‘local’ (i.e. linkage to genes influencing fitness) and/or ‘general’ (genome‐wide heterozygosity) effects. We found a significant negative relationship between parental genetic relatedness and hatching success, and maternal heterozygosity was positively associated with offspring body size. The characteristics of the studied populations (recent admixture, polygynous matings) together with the fact that we found evidence for identity disequilibrium across our set of neutral markers suggest that HFCs may have resulted from genome‐wide inbreeding depression. However, one locus (Ase18) had disproportionately large effects on the observed HFCs: heterozygosity at this locus had significant positive effects on hatching success and offspring size. It suggests that this marker may lie near to a functional locus under selection (i.e. a local effect) or, alternatively, heterozygosity at this locus might be correlated to heterozygosity across the genome due to the extensive ID found in our populations (i.e. a general effect). Collectively, our results lend support to both the general and local effect hypotheses and reinforce the view that HFCs lie on a continuum from inbreeding depression to those strictly due to linkage between marker loci and genes under selection.     

Heterozygosity and lungworm burden in harbour seals (Phoca vitulina)

In several studies, heterozygosity measured at around 10 microsatellite markers correlates with parasite load. Usually the effect size is small, but while this may reflect reality, it may also be possible that too few markers are used or the measure of fitness contains too much error to reveal what is actually a much stronger underlying effect. Here, we analysed over 200 stranded harbour seals (Phoca vitulina) for an association between lungworm burden and heterozygosity, conducting thorough necropsies on the seals and genotyping the samples obtained for 27 microsatellites. We found that homozygosity predicts higher worm burdens, but only in young animals, where the worms have the greatest impact on fitness. Testing each locus separately, we found that a significant majority reveal a weak but similar trend for heterozygosity to be protective against high lungworm burden, suggesting a genome-wide effect, that is, inbreeding. This conclusion is supported by the fact that heterozygosity is correlated among markers in young animals but not in otherwise equivalent older ones. Taken as a whole, our results support the notion that homozygosity increases susceptibility to parasitic infection and suggest that parasites can be effective in removing inbred individuals from the population.     

Heterozygosity correlates with body size,nest site quality and productivity in a colonial waterbird,the whiskered tern (Chlidonias hybrida,Aves: Sternidae)

Positive effects of individual heterozygosity on naturally selected traits have been reported in wild populations of many animal taxa. The aim of this study was to test whether heterozygosity predicts the quality of acquired nest sites and productivity in a colonially breeding waterbird, the whiskered tern (Chlidonias hybrida). For this purpose, 40 adult terns from a small, recently established population in Central Poland were typed at eight microsatellite loci. We demonstrate that individual heterozygosity is positively related to hatching success. We hypothesize that this association could be mediated by direct effects of heterozygosity on the competitive abilities of individuals. We found that more heterozygous terns tended to breed in better protected central parts of the colony, suggesting that they had capabilities of outcompeting less heterozygous individuals and relegating them to the less attractive peripheries of the colony. It was also demonstrated that the link between heterozygosity and individual abilities to acquire more attractive nest site could be mediated by the larger size of heterozygous individuals. Although no correlations between heterozygosity and different components of condition were found, there was a positive association between female heterozygosity and both clutch size and egg size. We suggest that demonstrated heterozygosity‐fitness correlations could be primarily caused by inbreeding depression in the studied whiskered tern population.     

What animals do not do or fail to find: A novel observational approach for studying cognition in the wild

To understand how our brain evolved and what it is for, we are in urgent need of knowledge about the cognitive skills of a large variety of animal species and individuals, and their relationships to rapidly disappearing social and ecological conditions. But how do we obtain this knowledge? Studying cognition in the wild is a challenge. Field researchers (and their study subjects) face many factors that can easily interfere with their variables of interest. Although field studies of cognition present unique challenges, they are still invaluable for understanding the evolutionary drivers of cognition. In this review, I discuss the advantages and urgency of field‐based studies on animal cognition and introduce a novel observational approach for field research that is guided by three questions: (a) what do animals fail to find?, (b) what do they not do?, and (c) what do they only do when certain conditions are met? My goal is to provide guidance to future field researchers examining primate cognition.     

Cyclosporin A: a powerful immunosuppressant.

Cyclosporin A (CyA) is a powerful immunosuppressive agent whose lack of myelotoxicity makes it unique among nonsteroidal drugs currently given for immunosuppression. It has been used with initial success in recipients of kidney, liver, bone marrow and pancreas transplants, and it may also have clinical application in the treatment of autoimmune disorders. In regard to its use in transplant recipients, there are many remaining questions about its mechanism of action, the optimum dose, whether it should be used alone or with other immunosuppressants, whether it can suppress chronic rejection and what its long-term side effects may be. These questions can only be answered by further careful laboratory investigation and controlled clinical trials. Until then, CyA should only be administered in centres experienced in its use.     

Females prefer the scent of outbred males: good-genes-as-heterozygosity?

Background  

There is increasing interest to determine the relative importance of non-additive genetic benefits as opposed to additive ones for the evolution of mating preferences and maintenance of genetic variation in sexual ornaments. The 'good-genes-as-heterozygosity' hypothesis predicts that females should prefer to mate with more heterozygous males to gain more heterozygous (and less inbred) offspring. Heterozygosity increases males' sexual ornamentation, mating success and reproduction success, yet few experiments have tested whether females are preferentially attracted to heterozygous males, and none have tested whether females' own heterozygosity influences their preferences. Outbred females might have the luxury of being more choosey, but on the other hand, inbred females might have more to gain by mating with heterozygous males. We manipulated heterozygosity in wild-derived house mice (Mus musculus musculus) through inbreeding and tested whether the females are more attracted to the scent of outbred versus inbred males, and whether females' own inbreeding status affects their preferences. We also tested whether infecting both inbred and outbred males with Salmonella would magnify females' preferences for outbred males.     

Ecology of sessile animals on sublittoral hard substrata: The need to measure variation

This paper concerns assemblages of sessile animals occupying shaded, commonly vertical hard substrata in the shallow subtidal zone. We are interested particularly in questions about the coexistence of species and about what influences their joint dynamics. We propose a conceptual model which focuses on variation in characteristics such as birth and death rates, competitive interactions and dispersal. We argue that, qualitatively, this model appears to be a satisfactory representation of the important characteristics of certain sessile assemblages. Further, we suggest that it may explain the coexistence of a large number of ecologically similar species in assemblages that appear in a sense ‘stable’ (but where assemblages at different sites differ in detail). There is support for this assertion from formal theoretical work on simpler versions of the model. It is not sufficient merely to argue that the model seems satisfactory or plausible, so we finally consider what kind of data is needed for the further development and testing of this kind of model.     

The Food Amount Rating Scale: Development,Reliability, and Validity

Objective: Implied in measures of binge eating is the assumption that individuals agree on what comprises a large amount of food. However, whether individuals estimate food amounts similarly or whether estimation of food amounts varies as a function of personal characteristics is unknown. The Food Amount Rating Scale (FARS) is a standardized set of stimuli for assessing individuals’ judgment of food amounts. Research Methods and Procedures: Two versions of the FARS were developed, and their psychometric properties were assessed. These versions are the same in all respects except that the rater is instructed to rate various food amounts for the average woman on Form W and for the average man on Form M. Results: Content validity was confirmed by 14 researchers and research assistants in the field of eating disorders. The FARS is a 24-item inventory with adequate test–retest reliability (Form W = 0.85; Form M = 0.87) and split–half reliability (Form W = 0.90; Form M = 0.89). Convergent validity is suggested by the finding that ratings for the average woman (Form W) were significantly higher than ratings for the average man (Form M). Discussion: The FARS is a psychometrically sound tool for use in basic research focused on identifying whether the subjective judgment of food amounts varies as a function of personal characteristics and in clinical research where it may be important to know how individuals judge food amounts.     

Predictability of heterozygosity scores and polymorphism information content values for rat genetic markers

Construction of a genetic linkage map of the laboratory rat, Rattus norvegicus, establishes the rat as a genetic model. Allele sizes were reported for 432 simple sequence length polymorphisms (SSLPs) genotyped in 12 different substrains belonging to nine different inbred strains of rats. However, these nine strains represent only a fraction of the more than 140 inbred strains available. If allele sizes are not known, alternative indices of markers' polymorphism content can be used, such as heterozygosity (H) and polymorphism information content (PIC). Here, we have determined heterozygosity scores and PIC values for all markers of the rat genetic linkage map, and we evaluate the predictability of the heterozygosity and the PIC values. Correlation analysis between the nine inbred strains reported for the rat map and ten test strains yielded r=0.42 and r=0.44 for heterozygosity and PIC values, respectively. While the correlation of the indices between the two groups of animals is low, these indices do provide a means of predicting whether a genetic marker will be informative in strains where allele sizes are not known.     

Town Mouse, Country Mouse: adaptation and adaptability in Mus domesticus (M. musculus domesticus)

The generally accepted idea that the house mouse is a single, world-wide species which owes its success largely to commensalism with man is wrong. There are at least five European and two Asian species lumped together under the name Mus musculus, plus another fourteen Asian species in the same genus. The house mouse of western Europe is the one that has been introduced to the Americas and Australasia, as well as being domesticated in the laboratory and ‘fancy’ strains; it is properly described as Mus domesticus. A complication of this particular species is the existence of chromosomal races involving the fusion of pairs of chromosomes, apparently at random. These races seem to be reproductively isolated from normal (2n = 40) mice. They have been described in southern Europe and northern Britain. Genetical studies of wild-living mice have shown the operation of powerful natural selection, contrary to earlier assumptions that most of the polymorphic variation in the species (especially that revealed by electrophoresis) was neutral. The effects of such selection are reduced (but not eliminated) by the deme structure of established mouse populations; this social structure is much less rigid than some laboratory experiments have suggested, because of opportunism by individual mice in replacing dead or debilitated animals, and filling new niches as these become available. Virtually every mouse population is unique, since a population tends to be founded by a small group of animals drawn from a genetically variable ancestral population. This differentiation has allowed laboratory workers to develop inbred strains with characteristic properties; it has also resulted in over 130 sub-species being described from wild caught animals. A substantial proportion of these latter have probably arisen by instant sub-speciation through the founder effect. This is well illustrated by the mice of the Faroe islands, which are often quoted as standard examples of extremely rapid evolution. The adaptive properties of the house mouse that have made it such an effective pest and such a good laboratory animal have enabled it to colonize habitats as different as Antarctic tundra and tropical atolls. The species is an ideal one for the general biological task of dissecting the traits that contribute to this adaptability; the material is largely available for this task in the diversity of local forms established in different habitats and characterized genetical varieties maintained in the laboratory. More is known about M. domesticus than any other mammal, except possibly man; the time is ripe for fusing laboratory work on reproduction, mortality, and behaviour with the information increasingly coming from field studies of wild-living animals.     

Polyandry in dragon lizards: inbred paternal genotypes sire fewer offspring

Multiple mating in female animals is something of a paradox because it can either be risky (e.g., higher probability of disease transmission, social costs) or provide substantial fitness benefits (e.g., genetic bet hedging whereby the likelihood of reproductive failure is lowered). The genetic relatedness of parental units, particularly in lizards, has rarely been studied in the wild. Here, we examined levels of multiple paternity in Australia's largest agamid lizard, the eastern water dragon (Intellagama lesueurii), and determined whether male reproductive success is best explained by its heterozygosity coefficient or the extent to which it is related to the mother. Female polyandry was the norm: 2/22 clutches (9.2%) were sired by three or more fathers, 17/22 (77.2%) were sired by two fathers, and only 3/22 (13.6%) clutches were sired by one father. Moreover, we reconstructed the paternal genotypes for 18 known mother–offspring clutches and found no evidence that females were favoring less related males or that less related males had higher fitness. However, males with greater heterozygosity sired more offspring. While the postcopulatory mechanisms underlying this pattern are not understood, female water dragons likely represent another example of reproduction through cryptic means (sperm selection/sperm competition) in a lizard, and through which they may ameliorate the effects of male‐driven precopulatory sexual selection.     

Isolation of polymorphic tetranucleotide microsatellite markers for the brown anole (Anolis sagrei)

Eleven polymorphic microsatellite markers have been developed for the brown anole, Anolis sagrei. The number of alleles range from five to 14 per locus with the observed heterozygosity ranging from 0.46 to 0.92. These markers will be useful for analysis of questions concerning population genetic structure and reproductive behaviour.