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Good zoos have four aims-to conserve species, educate the public, engage in research, and provide recreation-all of which can only be achieved when underpinned by high animal welfare standards. In this paper, we share the approach that The Royal Zoological Society of Scotland's (RZSS) Edinburgh Zoo and Highland Wildlife Park take to animal welfare. We highlight the role that animal welfare research, in collaboration with universities, has had in enabling the zoo to take an evidence-based approach to welfare and to put findings into practice. We share the collaborative process through which we developed and piloted the current animal welfare assessment tools, how they were validated, and how they were tested for reliability as part of a long-term collaboration between the Royal Zoological Society of Scotland and the University of Stirling: (1) the RZSS Welfare Assessment Tool, a 50-question animal welfare assessment adapted from the British and Irish Association of Zoos and Aquariums (BIAZA) Toolkit; and (2) the Stirling Toolkit, a package of evidence-based resources for behavioural-data collection. Our aim is to facilitate standardised, evidence-based approaches to assessing animal welfare which, when finalised, can be used collaboratively across zoos.
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Life history theory indicates that individuals/species with a slow pace of life invest more in acquired than innate immunity. Factors that decrease the pace of life and predict greater investment in acquired immunity include increased nutritional resources, increased pathogen exposure and decreased risk of extrinsic mortality. Common care behaviors given to sick individuals produce exactly these effects: provisioning increases nutritional resources; hygiene assistance increases disease exposure of carers; and protection can reduce the risk of extrinsic mortality to sick individuals. This study, therefore, investigated under what conditions care giving behaviors might impact immune strategy and pace of life. The study employed an agent-based model approach that simulated populations with varying levels of care giving, disease mortality, disease transmissibility, and extrinsic mortality, enabling measurements of how the immune strategy and age structure of the populations changed over evolutionary time. We used multiple regressions to examine the effects of these variables on immune strategy and the age structure of the population. The findings supported our predictions that care was selected for an acquired immunity. However, the pace of life did not slow as expected. Instead, the population shifted to a faster, but also more cost-intensive reproductive strategy in which care improved child survival by subsidizing the development of acquired immune responses.
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Introduction: The circadian clock influences many aspects of animal welfare including metabolism, breeding, and behavior. In most species, circadian clocks are internal clocks regulated by external environmental cues called zeitgebers. The most common zeitgebers are light/dark cycles, food, and temperature. However, within captive environments, animals can be housed at latitudes with different light/dark cycles than their natural habitat and most other zeitgebers are controlled by humans. The effects that modified zeitgebers have on captive animals' circadian and circannual rhythmicity is largely unknown. To explore this and potential welfare implications, we measured and analyzed observational behavioral data of zoo-housed giant pandas for one year utilizing live camera footage from six zoos across the world. The worldwide distribution of the zoos gives us the unique opportunity to investigate how housing giant pandas within and outside of their natural latitudinal range can affect circadian rhythmicity and behavior. Methods: Focal sampling was completed for 11 giant pandas each month for 12 consecutive months to gain an estimate of one circannual cycle. Within each month, we estimated one daylight or 24 h cycle of activity/behavior by conducting 10-min observation sessions systemically each hour the pandas were visible. Results: Zero-inflated negative binomial mixture models found that latitude is associated with activity levels, with pandas housed outside of their natural latitudinal range displaying less activity than those within their latitudinal range. Amount of daylight, temperature minimum, and temperature range were also associated with activity cycles, potentially acting as zeitgebers. An association between sexual-related and stereotypic behavioral cycles was found, with the circannual cycles fluctuating in synchrony throughout several points in a year. Discussion: These results indicate that changes to common zeitgebers and environmental conditions can influence circadian and circannual cycles. The widespread evolution of circadian rhythms suggests an adaptive advantage to possessing one in an environment with cyclical changes, allowing species to anticipate changes in their environment and respond accordingly. Therefore, although animals are highly adaptive, creating a captive environment that mimics the environmental conditions for which the animal has evolved can encourage naturalistic cycles that ultimately aid in promoting positive welfare states and increasing chances of successful breeding and conservation.
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Circadian and circannual cycles of behavior regulate many aspects of welfare including metabolism, breeding, and behavioral interactions. In this study, we aim to demonstrate how systematically determining circadian and circannual cycles can provide insight into animals' needs and be part of an evidence-based approach to welfare assessment. We measured and analyzed the observational behavioral data of 13 zoo-housed giant pandas (Ailuropoda melanoleuca), across life stages and between sexes, each month for one year using live camera footage from six zoos across the world. Our results indicate that life stage was associated with changes in overall activity, feeding, locomotion, and pacing, and that sex influenced scent anointing and anogenital rubbing. Overall, the circadian rhythms showed three peaks of activity, including a nocturnal peak, as seen in wild giant pandas. We also found associations between sexual-related, stereotypical/abnormal, and feeding behavior, which are possibly linked to the timing of migration of wild pandas, and elucidated the relationship between a mother and cub, finding that they concentrate maternal behaviors to mainly after closing hours. Understanding these cycle patterns can aid animal care staff in predicting changing needs throughout the day, year, and life cycle and preemptively provide for those needs to best avoid welfare concerns.
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Parasite infestations depend on multiple host-related and environmental factors. In the case of ectoparasites, which are exposed to the environment beyond the host, an impact of climate, expressed by seasonal or yearly variations, can be expected. However, long-term dynamics of ectoparasite infestations are rarely studied in nonhuman primates. We investigated the yearly variations in ectoparasite infestations of two small primates, the gray (Microcebus murinus) and the golden-brown (Microcebus ravelobensis) mouse lemur. For a more comprehensive evaluation, we also analyzed the potential effects of yearly and monthly climatic variation (temperature, rainfall) in addition to habitat, host sex, age, species, and body mass, on ectoparasite infestation. Individuals of both host species were sampled in two study sites within the Ankarafantsika National Park in northwestern Madagascar during several months (March-November) and across 4 years (2010, 2011, 2015, 2016). Our results show significant monthly and yearly variations in the infestation rates of three native ectoparasite taxa (Haemaphysalis spp. ticks, Schoutedenichia microcebi chigger mites, Lemurpediculus spp. sucking lice) and in ectoparasite species richness in both mouse lemur species. In addition, significant impacts of several host-related (species, sex, body mass) and environmental factors (habitat, temperature, rainfall) were found, but with differences in relevance for the different parasite taxa and partly deviating in their direction. Although some differences could be attributed to either permanent or temporary presence of the parasites on the host or to ecological differences between the host species, the lack of specific knowledge regarding the life cycle and microhabitat requirements of each parasite taxon precludes a complete understanding of the factors that determine their infestation dynamics. This study demonstrates the presence of yearly and monthly dynamics in lemur-parasite interactions in tropical, seasonal, dry deciduous forests in Madagascar, which call out for broad ecological long-term studies focusing both on primate hosts and their parasites.
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Cheirogaleidae , Animais , Madagáscar , Estações do Ano , Ecossistema , FlorestasRESUMO
Cysts and trophozoites of vestibuliferid ciliates and larvae of Strongyloides were found in fecal samples from captive orangutans Pongo pygmaeus and P. abelii from Czech and Slovak zoological gardens. As comparative material, ciliates from semi-captive mandrills Mandrillus sphinx from Gabon were included in the study. Phylogenetic analysis of the detected vestibuliferid ciliates using ITS1-5.8s-rRNA-ITS2 and partial 18S ribosomal deoxyribonucleic acid (rDNA) revealed that the ciliates from orangutans are conspecific with Balantioides coli lineage A, while the ciliates from mandrills clustered with Buxtonella-like ciliates from other primates. Morphological examination of the cysts and trophozoites using light microscopy did not reveal differences robust enough to identify the genera of the ciliates. Phylogenetic analysis of detected L1 larvae of Strongyloides using partial cox1 revealed Strongyloides stercoralis clustering within the cox1 lineage A infecting dogs, humans, and other primates. The sequences of 18S rDNA support these results. As both B. coli and S. stercoralis are zoonotic parasites and the conditions in captive and semi-captive settings may facilitate transmission to humans, prophylactic measures should reflect the findings.
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Mandrillus , Parasitos , Humanos , Animais , Cães , Pongo pygmaeus , Filogenia , Parasitos/genética , Pongo/genética , Primatas/genética , DNA Ribossômico/genéticaRESUMO
Sucking lice live in intimate association with their hosts and often display a high degree of host specificity. The present study investigated sucking lice of the genus Lemurpediculus from six mouse lemur (Microcebus) and two dwarf lemur (Cheirogaleus) species endemic to the island of Madagascar, considered a biodiversity hotspot. Louse phylogenetic trees were created based on cytochrome C oxidase subunit I (COI), elongation factor 1α (EF1α) and internal transcribed spacer 1 (ITS1) sequences. While clustering according to host species was generally observed for COI and ITS1, suggesting high host specificity of the examined lice, EF1α sequences alone did not distinguish between lice of different Microcebus species, possibly due to rather recent divergence. As bootstrap support for basal tree structure was rather low, further data are necessary to resolve the evolutionary history of louse-mouse lemur associations. Three new species of sucking lice are described: Lemurpediculus zimmermanni sp. Nov. From Microcebus ravelobensis, Lemurpediculus gerpi sp.nov. from Microcebus gerpi, and Lemurpediculus tsimanampesotsae sp. nov. from Microcebus griseorufus. These new species are compared with all known congeneric species and identifying features are illustrated for all known species of Lemurpediculus.
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Madagascar's flora and fauna have evolved in relative isolation since the island split from the African and Indian continents. When the last common ancestors of lemurs left Africa between 40 and 70 million years ago, they carried a subset of the viral diversity of the mainland population within them, which continued to evolve throughout the lemur radiation. Relative to other primate radiations, we know very little about the past or present viral diversity of lemurs, particularly mouse lemurs. Using high-throughput sequencing, we identified two gammaretroviruses and three betaretroviruses in the genomes of four species of wild mouse lemurs. The two gammaretroviruses and two betaretroviruses have not previously been described. One betaretrovirus was previously identified. All identified viruses are present in both Lorisiformes and Lemuriformes but absent from haplorrhine primates. The estimated ages of these viruses are consistent with the estimated divergence dates of the host lineages, suggesting they colonized the lemur genome after the Haplorrhine-Strepsirrhine split, but before the Lorisiformes-Lemuriformes split and before the colonization of Madagascar. The viral phylogenies connect multiple lineages of retroviruses from non-lemur and non-Madagascar-native species, suggesting substantial cross-species transmission occurred deep in the primate clade prior to its geographic dispersal. These phylogenies provide novel insights into known retroviral clades. They suggest that the origin of gammaretroviruses in rodents or bats may be premature and that the Jaagsiekte sheep virus clade may be older and more broadly distributed among mammals than previously thought.
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Background and objectives: The behavioural immune system (BIS) is a motivational system that facilitates the avoidance of pathogens and is thought to have evolved as a less costly mechanism to combat infectious diseases compared to the physiological immune system. The Parasite Stress Theory of Social Values predicts that authoritarianism and collectivist attitudes may impact the BIS by predisposing people to support disease control measures, including severe restrictions like lockdowns or stay-at-home orders. This study investigates the relationship between authoritarianism, collectivism and Covid-19 worry on support for lockdown measures during the Covid-19 pandemic. Methodology: A total of 187 UK participants were recruited to complete an online survey, which was administered between 22 June and 7 July 2020. The survey included measures of authoritarianism, collectivism, Covid-19 worry and support for lockdown measures. The data were analysed using moderated parallel mediation analysis. Results: Covid-19 worry had a direct effect on support for and enforcement of lockdown measures, but not on the idea that adherence to lockdown rules should be an individual choice. The relationship between Covid Worry and Support for and Enforcement of lockdown measures was not mediated by authoritarianism, nor was it moderated by Collectivism. Collectivism and Authoritarianism were related to increased levels of support for lockdown independently from Covid Worry but were not related to enforcement. Conclusions and implications: Support for lockdown restrictions and enforcement was mainly associated with covid worry. Our findings do not support the parasite stress theory of social values and indicate that the BIS manifested in a more direct way, and not through social values.
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Mammalian captive dietary specialists like folivores are prone to gastrointestinal distress and primate dietary specialists suffer the greatest gut microbiome diversity losses in captivity compared to the wild. Marmosets represent another group of dietary specialists, exudivores that eat plant exudates, but whose microbiome remains relatively less studied. The common occurrence of gastrointestinal distress in captive marmosets prompted us to study the Callithrix gut microbiome composition and predictive function through bacterial 16S ribosomal RNA V4 region sequencing. We sampled 59 wild and captive Callithrix across four species and their hybrids. Host environment had a stronger effect on the gut microbiome than host taxon. Wild Callithrix gut microbiomes were enriched for Bifidobacterium, which process host-indigestible carbohydrates. Captive marmoset guts were enriched for Enterobacteriaceae, a family containing pathogenic bacteria. While gut microbiome function was similar across marmosets, Enterobacteriaceae seem to carry out most functional activities in captive host guts. More diverse bacterial taxa seem to perform gut functions in wild marmosets, with Bifidobacterium being important for carbohydrate metabolism. Captive marmosets showed gut microbiome composition aspects seen in human gastrointestinal diseases. Thus, captivity may perturb the exudivore gut microbiome, which raises implications for captive exudivore welfare and calls for husbandry modifications.
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Microbioma Gastrointestinal , Animais , Bactérias/genética , Bifidobacterium/genética , Callithrix/genética , Fezes/microbiologia , Microbioma Gastrointestinal/genética , Mamíferos/genética , RNA Ribossômico 16S/genéticaRESUMO
The COVID-19 pandemic has revealed an urgent need for a comprehensive, multidisciplinary understanding of how healthcare systems respond successfully to infectious pathogens-and how they fail. This study contributes a novel perspective that focuses on the selective pressures that shape healthcare systems over evolutionary time. We use a comparative approach to trace the evolution of care-giving and disease control behaviours across species and then map their integration into the contemporary human healthcare system. Self-care and pro-health environmental modification are ubiquitous across animals, while derived behaviours like care for kin, for strangers, and group-level organizational responses have evolved via different selection pressures. We then apply this framework to our behavioural responses to COVID-19 and demonstrate that three types of conflicts are occurring: (1) conflicting selection pressures on individuals, (2) evolutionary mismatches between the context in which our healthcare behaviours evolved and our globalized world of today and (3) evolutionary displacements in which older forms of care are currently dispensed through more derived forms. We discuss the significance of understanding how healthcare systems evolve and change for thinking about the role of healthcare systems in society during and after the time of COVID-19-and for us as a species as we continue to face selection from infectious diseases.
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The media is a powerful force that can affect the welfare of the domiciled dog population. Dogs have long been in human stories and their depictions can create demand for the breeds shown. While previous research has found that this effect can last for up to ten years after the release of a movie, how this phenomenon occurs is unknown. This paper examines if how a dog is portrayed in a movie is associated with a subsequent change in American Kennel Club breed registrations for that breed. Following a systematic literature review, four key themes were identified in how dogs are portrayed in the media; dogs portrayed as heroes, as anthropomorphised, as embodying the ideals of Western societies (Whiteness and heteronormativity) and as boundaries between wilderness and human society. Forty movies from between 1930 to 2004 were analysed, resulting in 95 dog characters scored, and hierarchical multiple linear regression was run. Movies with dogs portrayed as heroes were followed by significant increases in the number of American Kennel Club breed registrations for the breed shown, while anthropomorphised dogs were followed by significant decreases in the number of dogs registered for up to five years after a movie's release. These results indicate that how dogs are portrayed may be an important driver of demand for breeds. Future work should investigate whether these portrayals may have negative welfare implications for real dogs by leading to owners having unrealistic expectations for dogs or increasing demand for dogs with in-breeding related disorders.
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Cruzamento , Cães , Filmes Cinematográficos , Animais , Humanos , Estados UnidosRESUMO
Female primates signal impending ovulation with a suite of sexual signals. Studies of these signals have focussed on visual, and to a lesser extent, acoustic signals, neglecting olfactory signals. We aimed to investigate the information content of female olfactory signals in captive olive baboons (Papio anubis) and relate these to the female fertile period. We studied eight adult females living in four groups at the CNRS Station de Primatologie, Rousset-sur-Arc, France. We used vaginal cytology to detect ovulation. We investigated the volatile component of odour signals using solid-phase microextraction and gas chromatography-mass spectrometry. We found a total of 74 volatile compounds, of which we tentatively identified 25, including several ketones, alcohols, aldehydes, terpenes, volatile fatty acids and hydrocarbons that have been identified in odour profiles of other primates. Our results show that vaginal odour intensity differs with sexual cycle stage suggesting that odour might play a role in signalling female baboon fertility. We found differences in vaginal odour between females living in all-female and in mixed sex groups but we could not distinguish the effects of group composition, female age and identity. This study of olfactory signalling improves our understanding of how female primates advertise their sexual receptivity.
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Fertilidade , Odorantes/análise , Percepção Olfatória/fisiologia , Papio anubis/fisiologia , Comportamento Sexual Animal , Vagina/química , Compostos Orgânicos Voláteis/análise , Animais , Feminino , OvulaçãoRESUMO
Eight species of ectoparasites were collected during 225 gray mouse lemur, Microcebus murinus (J. F. Miller), captures, in Ankarafantsika National Park, Madagascar, in 2010-2011. The ixodid tick, Haemaphysalis lemuris Hoogstraal, was the most common ectoparasite and was mostly represented by nymphs. Other ectoparasites recorded include the polyplacid sucking louse, Lemurpediculus madagascariensis Durden, Kessler, Radespiel, Zimmermann, Hasiniaina, and Zohdy; the ixodid tick, Haemaphysalis simplex Neumann; an undescribed laelapid mite in the genus Aetholaelaps; another laelapid belonging to the genus Androlaelaps; the chigger mite Schoutedenichia microcebi Stekolnikov; an undescribed species of atopomelid mite in the genus Listrophoroides; and an undescribed species of psoroptid mite in the genus Cheirogalalges. Except for the 2 species of ticks and 1 species of chigger, these ectoparasites may be host-specific to M. murinus. Total tick (H. lemuris and H. simplex) infestation was significantly greater in August than October, whereas louse (L. madagascariensis) infestation was significantly greater in October. There was no significant difference in tick infestations between male and female lemurs, but male lemurs had significantly more lice than female lemurs. Reproductive status was not a significant predictor of tick infestation in males and females.
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Cheirogaleidae/parasitologia , Ectoparasitoses/veterinária , Doenças dos Primatas/parasitologia , Animais , Ectoparasitoses/epidemiologia , Ectoparasitoses/parasitologia , Feminino , Madagáscar/epidemiologia , Masculino , Distribuição de Poisson , Prevalência , Doenças dos Primatas/epidemiologia , Estações do Ano , Fatores SexuaisRESUMO
Acoustic phenotypic variation is of major importance for speciation and the evolution of species diversity. Whereas selective and stochastic forces shaping the acoustic divergence of signaling systems are well studied in insects, frogs, and birds, knowledge on the processes driving acoustic phenotypic evolution in mammals is limited. We quantified the acoustic variation of a call type exchanged during agonistic encounters across eight distinct species of the smallest-bodied nocturnal primate radiation, the Malagasy mouse lemurs. The species live in two different habitats (dry forest vs. humid forest), differ in geographic distance to each other, and belong to four distinct phylogenetic clades within the genus. Genetically defined species were discriminated reliably on the phenotypic level based on their acoustic distinctiveness in a discriminant function analysis. Acoustic variation was explained by genetic distance, whereas differences in morphology, forest type, or geographic distance had no effect. The strong impact of genetics was supported by a correlation between acoustic and genetic distance and the high agreement in branching pattern between the acoustic and molecular phylogenetic trees. In sum, stochastic factors such as genetic drift best explained acoustic diversification in a social communication call of mouse lemurs.
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One of the striking features of human social complexity is that we provide care to sick and contagious individuals, rather than avoiding them. Care-giving is a powerful strategy of disease control in human populations today; however, we are not the only species which provides care for the sick. Widespread reports occurring in distantly related species like cetaceans and insects suggest that the building blocks of care for the sick are older than the human lineage itself. This raises the question of what evolutionary processes drive the evolution of such care in animals, including humans. I synthesize data from the literature to evaluate the diversity of care-giving behaviors and conclude that across the animal kingdom there appear to be two distinct types of care-behaviors, both with separate evolutionary histories: (1) social care behaviors benefitting a sick individual by promoting healing and recovery and (2) community health behaviors that control pathogens in the environment and reduce transmission within the population. By synthesizing literature from psychology, anthropology, and biology, I develop a novel hypothesis (Hominin Pathogen Control Hypothesis) to explain how these two distinct sets of behaviors evolved independently then merged in the human lineage. The hypothesis suggests that social care evolved in association with offspring care systems whereas community health behaviors evolved as a type of niche construction. These two types of behaviors merged in humans to produce complex, multi-level healthcare networks in humans. Moreover, each type of care increases selection for the other, generating feedback loops that selected for increasing healthcare behaviors over time. Interestingly, domestication processes may have contributed to both social care and community health aspects of this process.
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Members of the sucking louse genus Pedicinus are ectoparasites of cercopithecid primates in Africa, Asia, and Gibraltar. Pedicinus gabonensis n. sp. is described on the basis of adult male and female specimens collected from the mandrill (Mandrillus sphinx) in Gabon. The new species is compared morphologically with other members of the genus Pedicinus, and a nuclear elongation factor 1 alpha gene sequence is provided. Host associations and geographical distributions of the 18 previously recognized species of the genus and of P. gabonensis n. sp. are reviewed. Updated identification keys are provided for males and females of all known valid species of Pedicinus.
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Anoplura/classificação , Infestações por Piolhos/veterinária , Mandrillus/parasitologia , Doenças dos Macacos/parasitologia , Animais , Anoplura/anatomia & histologia , Anoplura/genética , Anoplura/fisiologia , DNA/química , DNA/isolamento & purificação , Feminino , Gabão/epidemiologia , Infestações por Piolhos/epidemiologia , Infestações por Piolhos/parasitologia , Masculino , Doenças dos Macacos/epidemiologia , Alinhamento de Sequência/veterinária , Análise de Sequência de DNA/veterináriaRESUMO
A new chigger mite species, Schoutedenichia microcebi n. sp. is described from the grey mouse lemur Microcebus murinus (J.F. Miller) from Madagascar. The new species is closely related to S. dutoiti (Radford, 1948), a species described from a single specimen collected on a rodent in South Africa. Examination of the holotype and new material on S. dutoiti from South Africa enabled us to re-describe this species and provide new data on its hosts and geographical distribution.
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Cheirogaleidae/parasitologia , Trombiculidae/classificação , Trombiculidae/fisiologia , Animais , Madagáscar , Camundongos , África do Sul , Especificidade da EspécieRESUMO
Humans are the only species to have evolved cooperative care-giving as a strategy for disease control. A synthesis of evidence from the fossil record, paleogenomics, human ecology, and disease transmission models, suggests that care-giving for the diseased evolved as part of the unique suite of cognitive and socio-cultural specializations that are attributed to the genus Homo. Here we demonstrate that the evolution of hominin social structure enabled the evolution of care-giving for the diseased. Using agent-based modeling, we simulate the evolution of care-giving in hominin networks derived from a basal primate social system and the three leading hypotheses of ancestral human social organization, each of which would have had to deal with the elevated disease spread associated with care-giving. We show that (1) care-giving is an evolutionarily stable strategy in kin-based cooperatively breeding groups, (2) care-giving can become established in small, low density groups, similar to communities that existed before the increases in community size and density that are associated with the advent of agriculture in the Neolithic, and (3) once established, care-giving became a successful method of disease control across social systems, even as community sizes and densities increased. We conclude that care-giving enabled hominins to suppress disease spread as social complexity, and thus socially-transmitted disease risk, increased.
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Evolução Biológica , Fósseis , Hominidae/fisiologia , Comportamento Social , Animais , HumanosRESUMO
Lemurpediculus madagascariensis sp. nov. (Phthiraptera: Anoplura: Polyplacidae) is described from the Gray Mouse lemur, Microcebus murinus (J. F. Miller) (Primates: Cheirogaleidae), from Ankarafantsika National Park, Madagascar. Lemurs were trapped using Sherman Live Traps and visually inspected for lice, which were preserved in 90% ethanol. Adults of both sexes and the third-instar nymph of the new species are illustrated and distinguished from the four previously known species of Lemurpediculus: L. verruculosus (Ward); L. petterorum Paulian; L. claytoni Durden, Blanco, and Seabolt; and L. robbinsi Durden, Blanco, and Seabolt. It is not known if the new species of louse is a vector of any pathogens or parasites.