Rachel L. Harris

Toward a Mechanistic Understanding of Environmentally Forced Zoonotic Disease Emergence: Sin Nombre Hantavirus

Abstract Understanding the environmental drivers of zoonotic reservoir and human interactions is crucial to understanding disease risk, but these drivers are poorly predicted. We propose a mechanistic understanding of human–reservoir interactions, using hantavirus pulmonary syndrome as a case study. Crucial processes underpinning the diseases incidence remain poorly studied, including the connectivity among natural and peridomestic deer mouse host activity, virus transmission, and human exposure. We found that disease cases were greatest in arid states and declined exponentially with increasing precipitation. Within arid environments, relatively rare climatic conditions (e.g., El Niño) are associated with increased rainfall and reservoir abundance, producing more frequent virus transmission and host dispersal. We suggest that deer mice increase their occupancy of peridomestic structures during spring–summer, amplifying intraspecific transmission and human infection risk. Disease incidence in arid states may increase with predicted climatic changes. Mechanistic approaches incorporating reservoir behavior, reservoir–human interactions, and pathogen spillover could enhance our understanding of global hantavirus ecology, with applications to other directly transmitted zoonoses.

Closing the gap on causal processes of infection risk from cross-sectional data: structural equation models to understand infection and co-infection

BackgroundEpidemiological studies of disease exposure risk are frequently based on observational, cross-sectional data, and use statistical approaches as crucial tools for formalising causal processes and making predictions of exposure risks. However, an acknowledged limitation of traditional models is that the inferred relationships are correlational, cannot easily distinguish direct from indirect determinants of disease risk, and are often considerable simplifications of complex interrelationships. This may be particularly important when attempting to infer causality in patterns of co-infection through pathogen-facilitation.MethodsWe describe analyses of cross-sectional data using structural equation models (SEMs), a contemporary advancement on traditional regression approaches, based on our study system of feline gammaherpesvirus (FcaGHV1) in domestic cats.ResultsSEMs strongly supported a latent (host phenotype) variable associated with FcaGHV1 exposure and co-infection risk, suggesting these individuals are simply more likely to become infected with multiple pathogens. However, indications of pathogen-covariance (potential facilitation) were also variably detected: potentially among FcaGHV1, Bartonella spp and Mycoplasma spp.ConclusionsOur models suggest multiple exposures are primarily driven by host phenotypic traits, such as aggressive male phenotypes, and secondarily by pathogen-pathogen interactions. The results of this study demonstrate the application of SEMs to understanding epidemiological processes using observational data, and could be used more widely as a complementary tool to understand complex cross-sectional information in a wide variety of disciplines.

The effectiveness of hair traps for surveying mammals: results of a study in sandstone caves in the Tasmanian southern midlands

We compared detection success of hair tubes and funnels with tape and Velcro adhesives as part of a small-scale mammal survey in sand-bottomed caves in the southern midlands of Tasmania. In order to detect small mammals entering traps but not leaving hair samples behind, a new type of funnel design was tested. In total, 19 species were detected throughout the survey period using a combination of hair traps and track and scat analysis. When tracks were observed inside funnel entrances no hairs were found on the adhesive tapes in 71% of cases. Hairs from several species were found in traps although there were no tracks of these species in the caves. These results further emphasise the importance of using multiple techniques when conducting general mammal surveys. Appropriate hair trap design is an important factor to be considered when conducting mammal surveys, as it has the potential to strongly influence survey efficiency and overall results.

Observations of breeding behaviour and possible infanticide in a wild population of Tasmanian echidnas ( Tachyglossus aculeatus setosus )

We describe field observations of Tasmanian echidna behaviour, including possible infanticide, where males damaged and entered nursery burrows. We also present the second report of a female producing a second offspring within a single reproductive season after the loss of her first young at an early stage.

MHC GENETIC VARIATION INFLUENCES BOTH OLFACTORY SIGNALS AND SCENT DISCRIMINATION IN RING-TAILED LEMURS

Diversity at the Major Histocompatibility Complex (MHC) is critical to health and fitness, such that MHC genotype may predict an individual’s quality or compatibility as a competitor, ally, or mate. Moreover, because MHC products can influence the components of bodily secretions, an individual’s body odor may signal its MHC and influence partner identification or mate choice. To investigate MHC-based signaling and recipient sensitivity, we test for odor-gene covariance and behavioral discrimination of MHC diversity and pairwise dissimilarity, under the good genes and good fit paradigms, in a strepsirrhine primate, the ring-tailed lemur (Lemur catta). First, we coupled genotyping with gas chromatography-mass spectrometry to investigate if diversity of the MHC-DRB gene is signaled by the chemical diversity of lemur genital scent gland secretions. We also assessed if the chemical similarity between individuals correlated with their MHC similarity. Next, we assessed if lemurs discriminated this chemically encoded, genetic information in opposite-sex conspecifics. We found that both sexes signaled overall MHC diversity and pairwise MHC similarity via genital secretions, but in a sex- and season-dependent manner. Additionally, both sexes discriminated absolute and relative MHC-DRB diversity in the genital odors of opposite-sex conspecifics, supporting previous findings that lemur genital odors function as advertisement of genetic quality. In this species, genital odors provide honest information about an individual’s absolute and relative MHC quality. Complementing evidence in humans and Old World monkeys, our results suggest that reliance on scent signals to communicate MHC quality may be important across the primate lineage.

Costs of injury for scent signalling in a strepsirrhine primate

Honesty is crucial in animal communication when signallers are conveying information about their condition. Condition dependence implies a cost to signal production; yet, evidence of such cost is scarce. We examined the effects of naturally occurring injury on the quality and salience of olfactory signals in ring-tailed lemurs (Lemur catta). Over a decade, we collected genital secretions from 23 (13 male, 10 female) adults across 34 unique injuries, owing primarily to intra-group fights. Using gas chromatography-mass spectrometry, we tested for differences in the chemical composition of secretions across pre-injury, injury and recovery, in animals that did and did not receive antibiotics. Lemur genital secretions were significantly dampened and altered during injury, with patterns of change varying by sex, season and antibiotics. Using behavioural bioassays (excluding odorants from antibiotic-treated animals), we showed that male ‘recipients’ discriminated injury status based on scent alone, directing more competitive counter marking towards odorants from injured vs. uninjured male ‘signallers.’ That injured animals could not maintain their normal signatures provides rare evidence of the energetic cost to signal production. That conspecifics detected olfactory-encoded ‘weakness’ suggests added behavioural costs: By influencing the likelihood of intra- or inter-sexual conflict, condition-dependent signals could have important implications for socio-reproductive behaviour.

Chemical Cues, Hibernation and Reproduction in Female Short-Beaked Echidnas ( Tachyglossus aculeatus setosus ): Implications for Sexual Conflict

The short-beaked echidna (Tachyglossus aculeatus) is a highly seasonal, usually solitary monotreme, and Australia’s most widely distributed native mammal. Tasmanian echidnas hibernate for several months of the year and show sexual conflict around the timing of mating, as males locate and attempt to mate with hibernating females. The effect of hibernation on chemical cues in mammals is poorly understood, but is potentially important in this system, since reproduction and hibernation overlap, and males use odor to locate females. Furthermore, females mate with multiple males throughout pregnancy, suggesting males cannot distinguish between pregnant and non-pregnant females. We combined chemical analyses of cloacal secretions with data from external temperature loggers, urogenital smears and behavioral observations collected from 35 female echidnas in a wild population over 3 years, to investigate the effects of hibernation and reproductive status on odor cues and mating activity. Odor cues varied between years, individuals and euthermic and hibernating animals. There were no detectable changes in scent profile composition after females entered hibernation, suggesting females do not produce a new, attractive odor cue while hibernating. Reproductive females showed mating activity before, during and after fertilization, but no concurrent changes in chemical profiles. Odor cues do not seem to advertise pregnancy to conspecifics, which could encourage multi-male mating and confuse paternity among males. We suggest the observed patterns of olfactory communication and mating behavior in this species are a product of interrelationships between environmental, physiological and demographic conditions.

Identification of desmostanol as a novel vertebrate sterol in short-beaked echidna secretions

Mass spectra and chromatographic data are presented to support the identification of cholest-24-en-3b-ol (desmostanol) in odorous secretions in Tasmanian short-beaked echidnas. This sterol has previously been described only in marine invertebrates and phytoplankton, and may have a role in chemical communication in the echidna.