Social inheritance of avoidances shapes the structure of animal social networks.

Social structure can have significant effects on selection, affecting both individual fitness traits and population-level processes. As such, research into its dynamics and evolution has spiked in the last decade, where theoretical and computational advances in social network analysis have increased our understanding of its ecological and inheritance underpinnings. Yet, the processes that shape the formation of structure within social networks are poorly understood and the role of social avoidances unknown. Social avoidances are an alternate of social affiliation in animal societies, which, although invisible, likely play a role in shaping animal social networks. Assuming social avoidances evolve under similar constraints as affiliative behavior, we extended a previous model of social inheritance of affiliations to investigate the impact of social inheritance of avoidances on social network structure. We modeled avoidances as relationships that individuals can copy from their mothers or from their mother's social environment and varied the degrees to which individuals inherit social affiliates and avoidances to test their combined influence on social network structure. We found that inheriting avoidances via maternal social environments made social networks less dense and more modular, thereby demonstrating how social avoidance can shape the evolution of animal social networks.

Influence of scat ageing on the gut microbiome: how old is too old?

BACKGROUND: The study of the host-microbiome by the collection of non-invasive samples has the potential to become a powerful tool for conservation monitoring and surveillance of wildlife. However, multiple factors can bias the quality of data recovered from scats, particularly when field-collected samples are used given that the time of defecation is unknown. Previous studies using scats have shown that the impact of aerobic exposure on the microbial composition is species-specific, leading to different rates of change in microbial communities. However, the impact that this aging process has on the relationship between the bacterial and fungal composition has yet to be explored. In this study, we measured the effects of time post-defecation on bacterial and fungal compositions in a controlled experiment using scat samples from the endangered koala (Phascolarctos cinereus). RESULTS: We found that the bacterial composition remained stable through the scat aging process, while the fungal composition did not. The absence of an increase in facultative anaerobes and the stable population of obligate anaerobic bacteria were likely due to our sampling from the inner portion of the scat. We report a cluster of fungal taxa that colonises scats after defecation which can dilute the genetic material from the autochthonous mycoflora and inhibit recovery. CONCLUSION: We emphasize the need to preserve the integrity of scat samples collected in the wild and combat the effects of time and provide strategies for doing so.

Whole-mitochondrial genomes of Nannizziopsis provide insights in evolution and detection.

Infectious fungal diseases can have devastating effects on wildlife health and a detailed understanding of the evolution of related emerging fungal pathogen along with the ability to detect them in the wild is considered indispensable for effective management strategies. Several fungi from the genera Nannizziopsis and Paranannizziopsis are emerging pathogens of reptiles and have been observed to cause disease in a wide range of taxa. Nannizziopsis barbatae has become a particularly important pathogen of Australian reptiles with an increasing number of herpetofauna being reported with cases of infection from across the country. Here, we present the mitochondrial genome sequences and phylogenetic analysis for seven species in this group of fungi uncovering new information on the evolutionary relationship of these emerging pathogens. From this analysis, we designed a species-specific qPCR assay for the rapid detection of N. barbatae and demonstrate its application in a wild urban population of a dragon lizard.

Post-whaling shift in mating tactics in male humpback whales.

Recent studies have shown behavioural plasticity in mating strategies can increase a population's ability to cope with anthropogenic impacts. The eastern Australian humpback whale population was whaled almost to extinction in the 1960s (~200 whales) and has recovered to pre-whaling numbers (>20,000 whales). Using an 18-year dataset, where the population increased from approximately 3,700 to 27,000 whales, we found that as male density increased over time, the use of mating tactics shifted towards more males engaging in non-singing physical competition over singing. Singing was the more successful tactic in earlier post-whaling years whereas non-singing behaviour was the more successful tactic in later years. Together, our study uncovers how changes in both local, and population-level male density resulted in a shift in the frequency, and fitness pay-off, of alternative mating tactics in a wild animal. This individual-level plasticity in male humpback whale mating tactics likely contributed to minimising their risk of extinction following a dramatic change in their social landscape due to whaling.

Selection in the city: Rapid and fine-scale evolution of urban eastern water dragons.

Oceanic archipelagos have long been treated as a Petri dish for studies of evolutionary and ecological processes. Like archipelagos, cities exhibit similar patterns and processes, such as the rapid phenotypic divergence of a species between urban and nonurban environments. However, on a local scale, cities can be highly heterogenous, where geographically close populations can experience dramatically different environmental conditions. Nevertheless, we are yet to understand the evolutionary and ecological implications for populations spread across a heterogenous cityscape. To address this, we compared neutral genetic divergence to quantitative trait divergence within three native riparian and four city park populations of an iconic urban adapter, the eastern water dragon. We demonstrated that selection is likely acting to drive divergence of snout-vent length and jaw width across native riparian populations that are geographically isolated and across city park populations that are geographically close yet isolated by urbanization. City park populations as close as 0.9 km exhibited signs of selection-driven divergence to the same extent as native riparian populations isolated by up to 114.5 km. These findings suggest that local adaptation may be occurring over exceptionally small geographic and temporal scales within a single metropolis, demonstrating that city parks can act as archipelagos for the study of rapid evolution.

Susceptibility to a sexually transmitted disease in a wild koala population shows heritable genetic variance but no inbreeding depression.

The koala, one of the most iconic Australian wildlife species, is facing several concomitant threats that are driving population declines. Some threats are well known and have clear methods of prevention (e.g., habitat loss can be reduced with stronger land-clearing control), whereas others are less easily addressed. One of the major current threats to koalas is chlamydial disease, which can have major impacts on individual survival and reproduction rates and can translate into population declines. Effective management strategies for the disease in the wild are currently lacking, and, to date, we know little about the determinants of individual susceptibility to disease. Here, we investigated the genetic basis of variation in susceptibility to chlamydia using one of the most intensively studied wild koala populations. We combined data from veterinary examinations, chlamydia testing, genetic sampling and movement monitoring. Out of our sample of 342 wild koalas, 60 were found to have chlamydia. Using genotype information on 5007 SNPs to investigate the role of genetic variation in determining disease status, we found no evidence of inbreeding depression, but a heritability of 0.11 (95% CI: 0.06-0.23) for the probability that koalas had chlamydia. Heritability of susceptibility to chlamydia could be relevant for future disease management, as it suggests adaptive potential for the population.

Testing the effectiveness of genetic monitoring using genetic non-invasive sampling.

Effective conservation requires accurate data on population genetic diversity, inbreeding, and genetic structure. Increasingly, scientists are adopting genetic non-invasive sampling (gNIS) as a cost-effective population-wide genetic monitoring approach. gNIS has, however, known limitations which may impact the accuracy of downstream genetic analyses. Here, using high-quality single nucleotide polymorphism (SNP) data from blood/tissue sampling of a free-ranging koala population (n = 430), we investigated how the reduced SNP panel size and call rate typical of genetic non-invasive samples (derived from experimental and field trials) impacts the accuracy of genetic measures, and also the effect of sampling intensity on these measures. We found that gNIS at small sample sizes (14% of population) can provide accurate population diversity measures, but slightly underestimated population inbreeding coefficients. Accurate measures of internal relatedness required at least 33% of the population to be sampled. Accurate geographic and genetic spatial autocorrelation analysis requires between 28% and 51% of the population to be sampled. We show that gNIS at low sample sizes can provide a powerful tool to aid conservation decision-making and provide recommendations for researchers looking to apply these techniques to free-ranging systems.

Microchromosomes are building blocks of bird, reptile, and mammal chromosomes.

Microchromosomes, once considered unimportant shreds of the chicken genome, are gene-rich elements with a high GC content and few transposable elements. Their origin has been debated for decades. We used cytological and whole-genome sequence comparisons, and chromosome conformation capture, to trace their origin and fate in genomes of reptiles, birds, and mammals. We find that microchromosomes as well as macrochromosomes are highly conserved across birds and share synteny with single small chromosomes of the chordate amphioxus, attesting to their origin as elements of an ancient animal genome. Turtles and squamates (snakes and lizards) share different subsets of ancestral microchromosomes, having independently lost microchromosomes by fusion with other microchromosomes or macrochromosomes. Patterns of fusions were quite different in different lineages. Cytological observations show that microchromosomes in all lineages are spatially separated into a central compartment at interphase and during mitosis and meiosis. This reflects higher interaction between microchromosomes than with macrochromosomes, as observed by chromosome conformation capture, and suggests some functional coherence. In highly rearranged genomes fused microchromosomes retain most ancestral characteristics, but these may erode over evolutionary time; surprisingly, de novo microchromosomes have rapidly adopted high interaction. Some chromosomes of early-branching monotreme mammals align to several bird microchromosomes, suggesting multiple microchromosome fusions in a mammalian ancestor. Subsequently, multiple rearrangements fueled the extraordinary karyotypic diversity of therian mammals. Thus, microchromosomes, far from being aberrant genetic elements, represent fundamental building blocks of amniote chromosomes, and it is mammals, rather than reptiles and birds, that are atypical.

Lifetime stability of social traits in bottlenose dolphins.

Behavioral phenotypic traits or "animal personalities" drive critical evolutionary processes such as fitness, disease and information spread. Yet the stability of behavioral traits, essential by definition, has rarely been measured over developmentally significant periods of time, limiting our understanding of how behavioral stability interacts with ontogeny. Based on 32 years of social behavioral data for 179 wild bottlenose dolphins, we show that social traits (associate number, time alone and in large groups) are stable from infancy to late adulthood. Multivariate analysis revealed strong relationships between these stable metrics within individuals, suggesting a complex behavioral syndrome comparable to human extraversion. Maternal effects (particularly vertical social learning) and sex-specific reproductive strategies are likely proximate and ultimate drivers for these patterns. We provide rare empirical evidence to demonstrate the persistence of social behavioral traits over decades in a non-human animal.

Repeatability and heritability of social reaction norms in a wild agamid lizard.

In the evolutionary transition from solitary to group living, it should be adaptive for animals to respond to the environment and choose when to socialize to reduce conflict and maximize access to resources. Due to the associated proximate mechanisms (e.g. neural network, endocrine system), it is likely that this behavior varies between individuals according to genetic and non-genetic factors. We used long-term behavioral and genetic data from a population of eastern water dragons (Intellagama lesueurii) to explore variation in plasticity of social behavior, in response to sex ratio and density. To do so, we modeled individual variation in social reaction norms, which describe individuals' mean behavior and behavioral responses to changes in their environment, and partitioned variance into genetic and non-genetic components. We found that reaction norms were repeatable over multiple years, suggesting that individuals consistently differed in their behavioral responses to changes in the social environment. Despite high repeatability of reaction norm components, trait heritability was below our limit of detection based on power analyses (h2 < 0.12), leading to very little power to detect heritability of plasticity. This was in contrast to a relatively greater amount of variance associated with environmental effects. This could suggest that mechanisms such as social learning and frequency-dependence may shape variance in reaction norms, which will be testable as the dataset grows.

Maternal effects and fitness consequences of individual variation in bottlenose dolphins' ecological niche.

The niche describes the ecological and social environment that an organism lives in, as well as the behavioural tactics used to interact with its environment. A species niche is key to both ecological and evolutionary processes, including speciation, and has therefore been a central focus in ecology. Recent evidence, however, points to considerable individual variation in a species' or population's niche use, although how this variation evolves or is maintained remains unclear. We used a large longitudinal dataset to investigate the drivers and maintenance of individual variation in bottlenose dolphins' Tursiops aduncus niche. Specifically, we (a) characterised the extent of individual differences in habitat use, (b) identified whether there were maternal effects associated with this variation and (c) investigated the relationship between habitat use and calving success, a component of reproductive fitness. By examining patterns of habitat use, we provide evidence that individual dolphins vary consistently between one another in their niche. We further show that such individual variation is driven by a strong maternal effect. Finally, habitat use and calving success were not related, suggesting that use of different habitats results in similar fitness outcomes. Niche partitioning, maintained by maternal effects, likely facilitates the coexistence of multiple ecotypes within this population.

Genome Sequence of the Fungus Nannizziopsis barbatae, an Emerging Reptile Pathogen.

Nannizziopsis barbatae is an emerging fungal pathogen capable of causing contagious dermatomycosis in reptiles. Here, we report a 31.54-Mb draft genome sequence of an isolate originating from an infected eastern water dragon in Brisbane, Australia.

Cross-continental emergence of Nannizziopsis barbatae disease may threaten wild Australian lizards.

Members of the genus Nannizziopsis are emerging fungal pathogens of reptiles that have been documented as the cause of fatal mycoses in a wide range of reptiles in captivity. Cases of severe, proliferative dermatitis, debility and death have been detected in multiple free-living lizard species from locations across Australia, including a substantial outbreak among Eastern water dragons (Intellagama lesueurii) in Brisbane, Queensland. We investigated this disease in a subset of severely affected lizards and identified a clinically consistent syndrome characterized by hyperkeratosis, epidermal hyperplasia, dermal inflammation, necrosis, ulceration, and emaciation. Using a novel fungal isolation method, histopathology, and molecular techniques, we identified the etiologic agent as Nannizziopsis barbatae, a species reported only once previously from captive lizards in Australia. Here we report severe dermatomycosis caused by N. barbatae in five species of Australian lizard, representing the first cases of Nannizziopsis infection among free-living reptiles, globally. Further, we evaluate key pathogen and host characteristics that indicate N. barbatae-associated dermatomycosis may pose a concerning threat to Australian lizards.

Fitness benefits of male dominance behaviours depend on the degree of individual inbreeding in a polyandrous lizard.

In polyandrous species, sexual selection extends beyond mating competition to selection for egg fertilization. As a result, the degree to which factors influencing mating success impact overall reproductive success becomes variable. Here, we used a longitudinal behavioural and genetic dataset for a population of eastern water dragons (Intellagama lesueurii) to investigate the degree to which male dominance, a pre-mating selection trait, influences overall reproductive success, measured as the number of surviving offspring. Moreover, we examine the interactive effects with a genetic trait, individual inbreeding, known to influence the reproductive success of males in this species. We found fitness benefits of male dominance, measured as body size and frequency of dominance behaviours displayed. However, individuals' propensity to display dominance behaviours had mixed effects, depending on the degree of inbreeding. While inbred males benefited from frequent displays, highly outbred males exhibited better reproductive outputs when displaying to a lesser extent. Given that outbred males have enhanced reproductive success in this species, the costs of displaying dominance behaviours may outweigh the benefits. Overall, our results demonstrate the fitness benefits of dominance in a polyandrous lizard, and suggest that these are modulated by an independent genetic trait. Our results may contribute to explaining the presence of alternative mating tactics in this species, owing to the variability in net fitness benefits of dominance. Our findings also reveal the challenges associated with investigating fitness traits in isolation, which may undermine the validity of results when important interactions are ignored.

Inbreeding and disease avoidance in a free-ranging koala population.

Habitat destruction and fragmentation are increasing globally, forcing surviving species into small, isolated populations. Isolated populations typically experience heightened inbreeding risk and associated inbreeding depression and population decline; although individuals in these populations may mitigate these risks through inbreeding avoidance strategies. For koalas, as dietary specialists already under threat in the northern parts of their range, increased habitat fragmentation and associated inbreeding costs are of great conservation concern. Koalas are known to display passive inbreeding avoidance through sex-biased dispersal, although population isolation will reduce dispersal pathways. We tested whether free-ranging koalas display active inbreeding avoidance behaviours. We used VHF tracking data, parentage reconstruction, and veterinary examination results to test whether free-ranging female koalas avoid mating with (a) more closely related males; and (b) males infected with sexually transmitted Chlamydia pecorum. We found no evidence that female koalas avoid mating with relatively more related available mates. In fact, as the relatedness of potential mates increases, so did inbreeding events. We also found no evidence that female koalas can avoid mating with males infected with C. pecorum. The absence of active inbreeding avoidance mechanisms in koalas is concerning from a conservation perspective, as small, isolated populations may be at even higher risk of inbreeding depression than expected. At risk koala populations may require urgent conservation interventions to augment gene flow and reduce inbreeding risks. Similarly, if koalas are not avoiding mating with individuals with chlamydial disease, populations may be at higher risk from disease than anticipated, further impacting population viability.

Quantifying koala locomotion strategies: implications for the evolution of arborealism in marsupials.

The morphology and locomotor performance of a species can determine their inherent fitness within a habitat type. Koalas have an unusual morphology for marsupials, with several key adaptations suggested to increase stability in arboreal environments. We quantified the kinematics of their movement over ground and along narrow arboreal trackways to determine the extent to which their locomotion resembled that of primates, occupying similar niches, or basal marsupials from which they evolved. On the ground, the locomotion of koalas resembled a combination of marsupial behaviours and primate-like mechanics. For example, their fastest strides were bounding type gaits with a top speed of 2.78 m s-1 (mean 1.20 m s-1), resembling marsupials, while the relatively longer stride length was reflective of primate locomotion. Speed was increased using equal modification of stride length and frequency. On narrow substrates, koalas took longer but slower strides (mean 0.42 m s-1), adopting diagonally coupled gaits including both lateral and diagonal sequence gaits, the latter being a strategy distinctive among arboreal primates. The use of diagonally coupled gaits in the arboreal environment is likely only possible because of the unique gripping hand morphology of both the fore and hind feet of koalas. These results suggest that during ground locomotion, they use marsupial-like strategies but alternate to primate-like strategies when moving amongst branches, maximising stability in these environments. The locomotion strategies of koalas provide key insights into an independent evolutionary branch for an arboreal specialist, highlighting how locomotor strategies can convergently evolve between distant lineages.

City life alters the gut microbiome and stable isotope profiling of the eastern water dragon (Intellagama lesueurii).

Urbanisation is one of the most significant threats to biodiversity, due to the rapid and large-scale environmental alterations it imposes on the natural landscape. It is, therefore, imperative that we understand the consequences of and mechanisms by which, species can respond to it. In recent years, research has shown that plasticity of the gut microbiome may be an important mechanism by which animals can adapt to environmental change, yet empirical evidence of this in wild non-model species remains sparse. Using an empirical replicated study system, we show that city life alters the gut microbiome and stable isotope profiling of a wild native non-model species - the eastern water dragon (Intellagama lesueurii) in Queensland, Australia. City dragons exhibit a more diverse gut microbiome than their native habitat counterparts and show gut microbial signatures of a high fat and plant rich diet. Additionally, we also show that city dragons have elevated levels of the Nitrogen-15 isotope in their blood suggesting that a city diet, which incorporates novel anthropogenic food sources, may also be richer in protein. These results highlight the role that gut microbial plasticity plays in an animals' response to human-altered landscapes.

Is MHC diversity a better marker for conservation than neutral genetic diversity? A case study of two contrasting dolphin populations.

Genetic diversity is essential for populations to adapt to changing environments. Measures of genetic diversity are often based on selectively neutral markers, such as microsatellites. Genetic diversity to guide conservation management, however, is better reflected by adaptive markers, including genes of the major histocompatibility complex (MHC). Our aim was to assess MHC and neutral genetic diversity in two contrasting bottlenose dolphin (Tursiops aduncus) populations in Western Australia-one apparently viable population with high reproductive output (Shark Bay) and one with lower reproductive output that was forecast to decline (Bunbury). We assessed genetic variation in the two populations by sequencing the MHC class II DQB, which encompasses the functionally important peptide binding regions (PBR). Neutral genetic diversity was assessed by genotyping twenty-three microsatellite loci. We confirmed that MHC is an adaptive marker in both populations. Overall, the Shark Bay population exhibited greater MHC diversity than the Bunbury population-for example, it displayed greater MHC nucleotide diversity. In contrast, the difference in microsatellite diversity between the two populations was comparatively low. Our findings are consistent with the hypothesis that viable populations typically display greater genetic diversity than less viable populations. The results also suggest that MHC variation is more closely associated with population viability than neutral genetic variation. Although the inferences from our findings are limited, because we only compared two populations, our results add to a growing number of studies that highlight the usefulness of MHC as a potentially suitable genetic marker for animal conservation. The Shark Bay population, which carries greater adaptive genetic diversity than the Bunbury population, is thus likely more robust to natural or human-induced changes to the coastal ecosystem it inhabits.

Individual Variation in the Social Plasticity of Water Dragons.

Individuals should alter when they socially associate with conspecifics to avoid potentially costly interactions. Moreover, individuals may vary in their propensity to use information about conspecifics when making such social decisions. However, surprisingly little is known about either the determinants of or the individual variation in such "social plasticity." We show here that eastern water dragons (Intellegama lesueurii lesueurii) may simultaneously use information from different components of their social environment when deciding whether to socially associate. In particular, we found that individuals altered when they socially associated with conspecifics according to the levels of potential conflict and competition in their social environment; both sexes socially associated more at higher local density than would be expected under increased random encounters. Further, females were more likely to socially associate during the breeding season and when there were more males and/or conspecifics whom they typically avoided in their social environment. This suggests that females may seek safety in numbers when the potential for intrasexual conflict or sexual harassment is high. Using a behavioral reaction norm framework, we also provide novel evidence to show that individuals vary in the extent and direction of their social plasticity and that males varied more than females. Our study thus implies that individuals use multiple cues in their environment when deciding to socially associate and that the resulting social plasticity varies between the sexes and between individuals.