Adult Empathy: Possible Gender Differences in Gene-Environment Architecture for Cognitive and Emotional Components in a Large Italian Twin Sample.

Empathy plays a central role in prosocial behavior and human cooperation. Very few twin researchers have investigated innate and environmental effects in adult empathy, and twin research on gender differences in these effects is sparse. The goal of this study was to examine innate and environmental influences on three components of an empathy scale frequently used with adults - the expression of cognitive (CE), emotional (EE), and social skills (SS) empathy - and to explore gender differences in the influences. Study participants were ~1,700 twins (18-65 years) enrolled in the Italian Twin Registry. Empathy was assessed with the Italian version of the Empathy Quotient (EQ), for which the three-factor structure (i.e., CE, EE, and SS) was confirmed. Twin correlations in monozygotic and dizygotic pairs, and males and females were estimated for the total EQ and subscale scores, and univariate genetic model fitting was carried out. Women's empathy (i.e., total EQ as well as CE and EE subdimensions) was predominantly driven by genetic factors and individual experiences, whereas for males, no genetic contribution or important shared and individual environmental effects emerged. Although of large magnitude, the gender differences did not reach statistical significance. Age did not moderate empathy heritability in adulthood. Only for the SS subscale were genetic and environmental proportions of variance similar for men and women. This study suggests possible gender-specific innate and environmental influences on empathy and its cognitive and emotional components that need to be confirmed in future studies.

A Behavioural Case Study of Early Social Isolation of a Subadult White-Handed Gibbon (Hylobates lar).

Our aim in this study was to analyse the effects of early social isolation on the behaviour of a white-handed gibbon (Hylobates lar) and at the same time to improve his level of welfare. The subject was a 6-year-old male, isolated from conspecific as well as other non-human primates since he was 3 months old. We presented the gibbon with a series of species-specific vocalisations, and we then introduced a 23-year-old conspecific female into his cage. Our subject did not respond to playbacks, whereas he immediately interacted positively with the conspecific female. After 2 days of presentation, the pair started to spend time in proximity to each other and initiated grooming through the wire-mesh dividing the cages. Four days later we recorded vocal duets. No obvious ste-reotypic behaviours were observed, and the prolonged isolation did not seem to compromise the ability of the young gibbon to socialise with the female conspecific. It appears that prolonged isolation does not always compromise the possibility of recovering socially in a satisfactory manner.

Exchanging grooming, but not tolerance and aggression in common marmosets (Callithrix jacchus).

In this study, we investigated the reciprocal exchanges of grooming, tolerance and reduced aggression in common marmosets (Callithrix jacchus), a cooperatively breeding primate whose groups are typically characterized by uniformly high genetic relatedness and high interdependency between group members. Both partner control and partner choice processes played a role in the reciprocal exchanges of grooming. In contrast, we did not find any evidence of reciprocity between grooming and tolerance over a preferred food source or between grooming and reduced aggression. Thus, reciprocity seems to play a variable role in the exchange of cooperative behaviors in marmosets.

Promoting Good Nonhuman Primate Welfare outside Regular Working Hours.

Promoting good primate welfare outside of daylight hours is an important task. The responsibility to provide a complex environment and environmental enrichment is an essential element of primate wellbeing programs that should be approached from a 24-h perspective and planned according to the species and individual needs, including giving animals the ability to interact with and control their environment during hours when animal care staff are not present. One must be aware, however, that their needs may differ at night-time from their care needs during the day when staff are present. Assessing welfare and providing enrichment during times when staff are not on hand can be achieved through the use of a variety of technologies, such as night-view cameras, animal-centred technologies, and data loggers. This paper will address the relevant topics concerning the care and welfare of primates during off-hours, and the use of related technologies to facilitate and assess wellbeing at these times.

Monomorphic region of the serotonin transporter promoter gene in New World monkeys.

Genetic variation in the human serotonin system has long been studied because of its functional consequences and links to various neuropsychiatric and behavior-related disorders. Among non-human primates, the common marmosets (Callithrix jacchus) and tufted capuchins monkeys (Cebus apella) are becoming increasingly used as models to study the effects of genes, environments, and their interaction on physiology and complex behavior. In order to investigate the independent functions of and potential interactions between serotonin-related genes, anxiety and neuropsychiatric disorders, we analyzed the presence and variability of the serotonin transporter gene-linked polymorphic region (5-HTTLPR) in marmoset and capuchin monkeys. By PCR and using heterologous primers from the human sequence, we amplified and then sequenced the corresponding 5-HTT region in marmosets and capuchins. The resulting data revealed the presence of a tandem repeat sequence similar to that described in humans, but unlike humans and other Old World primates, no variable length alleles were detected in these New World monkeys, suggesting that if serotonin transporter is involved in modulating behavior in these animals it does so through different molecular mechanisms.

The principle of the 3Rs between aspiration and reality.

The Principle of the 3Rs is widely recognised as the methodological and ethical backbone of contemporary animal research. Different authors also stress the reciprocal links among the 3Rs, and how these often complement and reinforce each other. We very much agree with this point, but in this contribution we would like to raise some problems related to the application of the "3Rs". There is an obvious link among "Replacement, "Reduction" and "Refinement", but it is worth to notice also that each "R" has its own conceptual characteristics, as well as its own level of applicability. For example, a realistic "methodological inertia" has to be expected more in the case of "Replacement" than in the case of "Refinement". This also leads to a second order of issues, and here we will offer our experience as projects evaluators. The "3Rs" differ also in the possibility to verify how are applied by the proponents of research protocols involving the use of animal models. Sometimes it appears that the application of the Principle still resolves itself in the use of formulaic sentences, from which it is difficult to really understand the reality of the laboratory decisional and procedural processes. However, the demanding characteristics of the "3Rs" can vary greatly, and this is something that has to be considered. We propose that a network, or a virtual platform, of evaluators could help both researchers and evaluators for a more satisfactory understanding and pragmatic application of the Principle of the 3Rs.

Primatology between feelings and science: a personal experience perspective.

The aim of this article is to discuss some aspects of the relationship between feelings and primatological science, and how this relationship can influence this particular scientific practice. This point of view is based on the author's personal experience. A sentimental reason to study primatology in the first place will be discussed, and then the existence of a bond between the observer and the observed will be presented as a possible by-product of primatology. The following question is whether a sentimental attitude toward primates is detrimental for good science or is, alternatively, actually leading to better primatological science. As an example, the practice of naming individual monkeys is considered. It is argued that naming monkeys can help by characterizing individuality, and this is likely to improve planning of behavioural observations and welfare of captive individuals. The relationship between the researcher and study subject in biomedical studies is discussed in terms of hierarchy of moral status. Finally, primatology is not unique in the existence of bonds between the observer and the observed, at least from the point of view of the observer. However, primatology is unique because, more than in other cases, it gives greater opportunity for reasoning about different factors surrounding "doing science with animals." This is most probably owing to the phylogenetic closeness primatologists have with their study subjects. Among the different factors involved in making science using animals, the sentimental bond developing between the researcher and study animal can be very influential.

Introduction to the special section: "the effects of bonds between human and nonhuman primates on primatological research and practice".

This commentary introduces this special section on ''the Effects of Bonds Between Human and Nonhuman Primates on Primatological Research and Practice.'' The aim is to explore the different causes and consequences of bonding experiences between observers and observed in different primatological contexts. In the first contribution, Vitale asks what are the possible consequences of such bonding in behavioral primatology. Examples of beneficial consequences of this kind of relationship come fromstudies on cognitive abilities of great apes. Furthermore, an empathic attitude with the experimental animals leads to better care and attention toward individual welfare needs. Coleman discusses the particular case of nonhuman primates housed in research laboratories. Care-giving practices arediscussed in relation to scientific, ethical and emotional issues. Morimura et al. present the case of the first Japanese sanctuary for retiring chimpanzees from research where, in order to facilitate the social living of re-located chimpanzees, face-to-face interactions between caregivers and chimpanzees areessential. Asquith discusses the role of an thropomorphism, and proposes that this attitude can help to better understand the lives of primates, in more contextualized scenarios. In relation to this view, sheemphasizes how the term ''primate culture'' accords with some definition of the term ''human culture.''Fuentes, in his article asks whether national, class and ethnic characteristics can influence bonding between human and nonhuman primates, and calls for focused quantitative studies. Finally, Rose calls for the application of the concept of biosynergy, explained as promoting the formation of healthy and sustainable bonding relationships among living creatures. One of the most important aspects emerging from these papers is the need to better understand whether the issue of bonding in primatological studiescan be generalized to other areas of research such as conservation, behavior, captive care, or whether each of these disciplines needs to develop their own understanding of the effects of bonding in ''producing science.''

The 3R principle and the use of non-human primates in the study of neurodegenerative diseases: the case of Parkinson's disease.

The aim of this paper is to offer an ethical perspective on the use of non-human primates in neurobiological studies, using the Parkinson's disease (PD) as an important case study. We refer, as theoretical framework, to the 3R principle, originally proposed by Russell and Burch [Russell, W.M.S., Burch, R.L., 1959. The Principles of Humane Experimental Technique. Universities Federation for Animal Welfare Wheathampstead, England (reprinted in 1992)]. Then, the use of non-human primates in the study of PD will be discussed in relation to the concepts of Replacement, Reduction, and Refinement. Replacement and Reduction result to be the more problematic concept to be applied, whereas Refinement offers relatively more opportunities of improvement. However, although in some cases the 3R principle shows its applicative limits, its value, as conceptual and inspirational tool remains extremely valuable. It suggests to the researchers a series of questions, both theoretical and methodological, which can have the results of improving the quality of life on the experimental models, the quality of the scientific data, and the public perception from the non-scientist community.

The application of Russell and Burch 3R principle in rodent models of neurodegenerative disease: the case of Parkinson's disease.

Currently, the accepted ethical standards for the regulation of animal experimentation are provided by the 3R principle (Replacement, Reduction and Refinement). The development of alternative methods to the use of animals (Replacement), the design of adequate experimental protocols to reduce the number of animals (Reduction), the application of refinement practices (Refinement) are all aspects to be considered to ensure ethical and scientific validity to animal experimentation. This review intends to address these issues, using experimental research on Parkinson's disease (PD) as a paradigmatic example of the use of animal models to improve knowledge on a devastating human pathology. In particular, current rodent models of PD and their validity are reviewed and discussed, and methodologies that may ultimately reduce animal's suffering emphasized. Although procedures referring to with 3R principle can be traced in the literature reviewed, they are not considered yet an important part of the methodological information. The formal inclusion in scientific papers of a section devoted to 3Rs may increase knowledge and eventually adherence to this principle by scientists.

Personality and lateralization in common marmosets (Callithrix jacchus).

Specialization of the left and right hemispheres to control behavioural responses may represent one of the mechanisms underlying individual differences in personality structure, as well as the preferential use of one hand. The present study investigated the relationship between personality and hand preference in common marmosets (Callithrix jacchus), a little New World monkey that presents highly consistent and stable individual hand preferences for simple reaching. To address this issue, data on 56 different behaviours from the species' behavioural repertoire were measured in 10 different laboratory tests and during observations under social conditions on 16 adult common marmosets. Stable behavioural variables were aggregated a priori into 13 personality traits. Exploratory Factor Analysis (EFA) on personality traits was carried out to verify the presence of major personality factors, and their relationship with direction and strength of individual hand preferences was assessed by multiple regression, taking into account sex and age of the subjects. The largest number of species-specific behaviours so far investigated in this species was taken into account and robust temporal stability between two testing periods was verified. We confirm that common marmosets are characterized by specific and stable personality profiles. A single personality factor, accounting for about 38% of the total variance, was found by EFA, that describes the interest towards unusual and new experiences and resembles the human Openness domain. The strength of the hand preference was found to be predicted by this personality factor, that we named Inquisitiveness. Present results highlight common marmoset as a useful primate model for the study of the relationship between personality and lateralization.

Polymorphism of the 3'-UTR of the dopamine transporter gene (DAT) in New World monkeys.

Genetic polymorphism in the 3'-untranslated region (3'-UTR) of the dopamine transporter (DAT) gene has been reported in both human and nonhuman primates, and the variable number of tandem repeats (VNTR) polymorphism has been related to several neurological and psychiatric disorders. As New World primates have been employed as models in biomedical research in these fields, in the present study we assessed genetic variation in the DAT gene in 25 robust capuchin monkeys (Sapajus spp.) and 39 common marmosets (Callithrix jacchus). Using enzymatic amplification followed by sequencing of amplified fragments, a VNTR polymorphism in the 3'-UTR region of the DAT gene was identified in both robust capuchins and common marmosets. The polymorphic tandem repeat of 40-bp basic units is similar to the human VNTR consensus sequence, with size variants composed of 9, 10, and 11 units in marmosets and 8, 9, 13, and 17 basic units in capuchins. We found behavioral evidence that carrying the 10-repeat DAT allele promotes flexible choice and maximization of foraging in marmosets tested in an operant choice paradigm. Moreover, in an intertemporal choice task, capuchins with longer repeat variants show less self-controlled choices than capuchins with at least one short repeat variant. Future research should focus on the relationship between these DAT polymorphisms, dopamine reuptake via the dopamine transporter, and behavioral and cognitive variation across New World monkey individuals.

EU guidelines for the care and welfare of an "exceptional invertebrate class" in scientific research. Commentary.

Cephalopods have been defined as "advanced invertebrates" due to the complexity of their nervous system and to their sophisticated behavioural repertoire. However, until recently, the protection and welfare of this class of invertebrates has been mostly disregarded by EU regulations on the use of laboratory animals. The inclusion of "live cephalopods" in the Directive 2010/63/EU has been prompted by new scientific knowledge on the "sentience" of animals used for experimental or other scientific purposes, a fundamental criterion to which animal species are included or not under the protective umbrella of the Directive. In this scenario, the imminent publication of the Guidelines for the care and welfare of cephalopods in research as an initiative by the CephRes-FELASA-Boyd Group is a sign of ethical progress in the consideration of animals in research, and is likely to have a significant impact on both scientific and practical aspects of research conducted with these animals.