skip to main content
Explore Scholarly Publications and Datasets in the NSF-PAR

  • NSF Public Access
  • Search Results
  • Accepted Manuscript: Sex, synchrony, and skin contact: integrating multiple behaviors to assess pathogen transmission risk
Title: Sex, synchrony, and skin contact: integrating multiple behaviors to assess pathogen transmission risk
Abstract Direct pathogen and parasite transmission is fundamentally driven by a population’s contact network structure and its demographic composition and is further modulated by pathogen life-history traits. Importantly, populations are most often concurrently exposed to a suite of pathogens, which is rarely investigated, because contact networks are typically inferred from spatial proximity only. Here, we use 5 years of detailed observations of Indo-Pacific bottlenose dolphins (Tursiops aduncus) that distinguish between four different types of social contact. We investigate how demography (sex and age) affects these different social behaviors. Three of the four social behaviors can be used as a proxy for understanding key routes of direct pathogen transmission (sexual contact, skin contact, and aerosol contact of respiratory vapor above the water surface). We quantify the demography-dependent network connectedness, representing the risk of exposure associated with the three pathogen transmission routes, and quantify coexposure risks and relate them to individual sociability. Our results suggest demography-driven disease risk in bottlenose dolphins, with males at greater risk than females, and transmission route-dependent implications for different age classes. We hypothesize that male alliance formation and the divergent reproductive strategies in males and females drive the demography-dependent connectedness and, hence, exposure risk to pathogens. Our more » study provides evidence for the risk of coexposure to pathogens transmitted along different transmission routes and that they relate to individual sociability. Hence, our results highlight the importance of a multibehavioral approach for a more complete understanding of the overall pathogen transmission risk in animal populations, as well as the cumulative costs of sociality. « less
Authors:
; ; ; ; ;
Editors:
Barrett, Louise
Award ID(s):
1755229
Publication Date:
NSF-PAR ID:
10199198
Journal Name:
Behavioral Ecology
Volume:
31
Issue:
3
Page Range or eLocation-ID:
651 to 660
ISSN:
1045-2249
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ( , Behavioral Ecology)
    Taborsky, Michael (Ed.)
    Abstract The juvenile period is a challenging life-history stage, especially in species with a high degree of fission–fusion dynamics, such as bottlenose dolphins, where maternal protection is virtually absent. Here, we examined how juvenile male and female bottlenose dolphins navigate this vulnerable period. Specifically, we examined their grouping patterns, activity budget, network dynamics, and social associations in the absence of adults. We found that juveniles live in highly dynamic groups, with group composition changing every 10 min on average. Groups were generally segregated by sex, and segregation was driven by same-sex preference rather than opposite-sex avoidance. Juveniles formed strong associations with select individuals, especially kin and same-sex partners, and both sexes formed cliques with their preferred partners. Sex-specific strategies in the juvenile period reflected adult reproductive strategies, in which the exploration of potential social partners may be more important for males (which form long-term alliances in adulthood) than females (which preferentially associate with kin in adulthood). Females spent more time alone and were more focused on foraging than males, but still formed close same-sex associations, especially with kin. Males cast a wider social net than females, with strong same-sex associations and many male associates. Males engaged in more affiliative behaviormore »than females. These results are consistent with the social bonds and skills hypothesis and suggest that delayed sexual maturity in species with relational social complexity may allow individuals to assess potential associates and explore a complex social landscape without the risks associated with sexual maturity (e.g., adult reproductive competition; inbreeding).« less
  2. ; ; ; ; ; ; ; ; ; ( , Frontiers in Marine Science)
    null (Ed.)
    As demands for wildlife tourism increase, provisioning has become a popular means of providing up-close viewing to the public. At Monkey Mia, Shark Bay, Australia, up to five adult female Indo-Pacific bottlenose dolphins ( Tursiops aduncus ) visit a 100 m stretch of beach daily to receive fish handouts. In 2011, a severe marine heatwave (MHW) devastated seagrass and fish populations in Shark Bay. Offspring survival declined precipitously among seagrass specialists (dolphins that forage disproportionately in seagrass habitat). As all provisioned dolphins at the site are seagrass specialists, we examined how provisioned and non-provisioned seagrass specialists responded to the MHW. Using 27 years of data we compare habitat use, home range size, calf mortality, and predation risk between provisioned and non-provisioned females and their offspring before and after the MHW. Our results show that provisioned females have extremely small home ranges compared to non-provisioned females, a pattern attributable to their efforts to remain near the site of fish handouts. However, weaned offspring (juveniles) born to provisioned females who are not provisioned themselves also had much smaller home ranges, suggesting a persistent maternal effect on their behavior. After the MHW, adult females increased their use of seagrass habitats, but not theirmore »home range size. Provisioned females had significantly lower calf mortality than non-provisioned females, a pattern most evident pre-MHW, and, in the first 5 years after the MHW (peri-MHW, 2011–2015), calf mortality did not significantly increase for either group. However, the ecosystem did not recover, and post-MHW (2016–2020), calf mortality was substantially higher, regardless of provisioning status. With few survivors, the impact of the MHW on juvenile mortality post-weaning is not known. However, over three decades, juvenile mortality among offspring of provisioned vs. non-provisioned females did not statistically differ. Thus, the survival benefits accrued to calves in the provisioned group likely cease after weaning. Finally, although shark attack rates on seagrass specialists did not change over time, elevated predation on calves cannot be ruled out as a cause of death post-MHW. We discuss our results as they relate to anthropogenic influences on dolphin behavioral plasticity and responses to extreme climate events.« less
  3. ; ; ( , mBio)
    Dubilier, Nicole (Ed.)
    ABSTRACT Endosymbionts can influence host reproduction and fitness to favor their maternal transmission. For example, endosymbiotic Wolbachia bacteria often cause cytoplasmic incompatibility (CI) that kills uninfected embryos fertilized by Wolbachia -modified sperm. Infected females can rescue CI, providing them a relative fitness advantage. Wolbachia -induced CI strength varies widely and tends to decrease as host males age. Since strong CI drives Wolbachia to high equilibrium frequencies, understanding how fast and why CI strength declines with male age is crucial to explaining age-dependent CI’s influence on Wolbachia prevalence. Here, we investigate if Wolbachia densities and/or CI gene ( cif ) expression covary with CI-strength variation and explore covariates of age-dependent Wolbachia -density variation in two classic CI systems. w Ri CI strength decreases slowly with Drosophila simulans male age (6%/day), but w Mel CI strength decreases very rapidly (19%/day), yielding statistically insignificant CI after only 3 days of Drosophila melanogaster adult emergence. Wolbachia densities and cif expression in testes decrease as w Ri-infected males age, but both surprisingly increase as w Mel-infected males age, and CI strength declines. We then tested if phage lysis, Octomom copy number (which impacts w Mel density), or host immune expression covary with age-dependent w Melmore »densities. Only host immune expression correlated with density. Together, our results identify how fast CI strength declines with male age in two model systems and reveal unique relationships between male age, Wolbachia densities, cif expression, and host immunity. We discuss new hypotheses about the basis of age-dependent CI strength and its contributions to Wolbachia prevalence. IMPORTANCE Wolbachia bacteria are the most common animal-associated endosymbionts due in large part to their manipulation of host reproduction. Many Wolbachia cause cytoplasmic incompatibility (CI) that kills uninfected host eggs. Infected eggs are protected from CI, favoring Wolbachia spread in natural systems and in transinfected mosquito populations where vector-control groups use strong CI to maintain pathogen-blocking Wolbachia at high frequencies for biocontrol of arboviruses. CI strength varies considerably in nature and declines as males age for unknown reasons. Here, we determine that CI strength weakens at different rates with age in two model symbioses. Wolbachia density and CI gene expression covary with w Ri-induced CI strength in Drosophila simulans , but neither explain rapidly declining w Mel-induced CI in aging D. melanogaster males. Patterns of host immune gene expression suggest a candidate mechanism behind age-dependent w Mel densities. These findings inform how age-dependent CI may contribute to Wolbachia prevalence in natural systems and potentially in transinfected systems.« less
  4. ; ; ; ; ; ; ( , Evolution, Medicine, and Public Health)
    Abstract Background

    Social isolation is a key risk factor for the onset and progression of age-related disease and mortality in humans. Nevertheless, older people commonly have narrowing social networks, with influences from both cultural factors and the constraints of senescence. We evaluate evolutionarily grounded models by studying social aging in wild chimpanzees, a system where such influences are more easily separated than in humans, and where individuals are long-lived and decline physically with age.

     Methodology

    We applied social network analysis to examine age-related changes in social integration in a 7+ year mixed-longitudinal dataset on 38 wild adult chimpanzees (22 females, 16 males). Metrics of social integration included social attractivity and overt effort (directed degree and strength), social roles (betweenness and local transitivity) and embeddedness (eigenvector centrality) in grooming networks.

     Results

    Both sexes reduced the strength of direct ties with age (males in-strength, females out-strength). However, males increased embeddedness with age, alongside cliquishness. These changes were independent of age-related changes in social and reproductive status. Both sexes maintained highly repeatable inter-individual differences in integration, particularly in mixed-sex networks.

     Conclusions and implications

    As in humans, chimpanzees appear to experience senescence-related declines in social engagement. However, male social embeddedness and overall sex differences were patterned more similarlymore »to humans in non-industrialized versus industrialized societies. Such comparisons suggest common evolutionary roots to ape social aging and that social isolation in older humans may hinge on novel cultural factors of many industrialized societies. Lastly, individual and sex differences are potentially important mediators of successful social aging in chimpanzees, as in humans.

    Lay summary: Few biological models explain why humans so commonly have narrowing social networks with age, despite the risk factor of social isolation that small networks pose. We use wild chimpanzees as a comparative system to evaluate models grounded in an evolutionary perspective, using social network analysis to examine changes in integration with age. Like humans in industrialized populations, chimpanzees had lower direct engagement with social partners as they aged. However, sex differences in integration and older males’ central positions within the community network were more like patterns of sociality in several non-industrialized human populations. Our results suggest common evolutionary roots to human and chimpanzee social aging, and that the risk of social isolation with age in industrialized populations stems from novel cultural factors.

    « less
  5. ; ; ; ; ; ( , American journal of physical anthropology)
    The socioecological model predicts that food availability and risk of parasite transmission influence sociality in primates. As a semi-solitary ape inhabiting the masting forests of Southeast Asia, orangutans provide a unique opportunity to compare social and non-social periods and highly variable foraging conditions within one population. This study compared two data collection periods when fruit availability differed markedly to determine whether sociality and parasite prevalence decrease as expected during periods of fruit scarcity. Fecal samples were analyzed using direct smear and fecal concentration techniques on-site at Cabang Panti Research Station from 2013-2014 and 2018-2019. From the high fruit period to the low fruit period, sociality decreased from 54% of focal follows containing a social event to 29%, while overall parasite prevalence remained the same at 100%. Interesting differences arose for certain parasite species, however. Enterobius sp. prevalence decreased during the low fruit period for both sexes but even more so for males (50% to 29% for females; 56% to 0 for males). Prevalence of Trichuris sp. increased for females during the low fruit period (5% to 43%) while prevalence among males remained the same. These results lend support to the prediction that social contact influences transmission risk for some parasitemore »species, while other parasites may be more responsive to factors such as changes in reproductive state. These findings suggest that differences in the behavioral strategies of the sexes and the differential energetic demands of life history stages have an influence on parasitic infection patterns.« less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email