Adam J. Stow

The impact of habitat fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites

The effects of habitat fragmentation on processes within and among populations are important for conservation management. Despite a broad spectrum of lifestyles and the conservation significance of many reptiles, very little work on fine‐scale population genetics has been carried out on this group. This study examines the dispersal patterns of a rock crevice‐dwelling lizard, Cunningham’s skink (Egernia cunninghami), in a naturally vegetated reserve and an adjacent deforested site. Both genotypic and genic approaches were employed, using microsatellite loci. The spatial organization of individuals with respect to pairwise relatedness coefficients and allele frequencies, along with assignment tests, were used to infer dispersal characteristics for both sexes in a natural and a cleared area. The distribution of relatedness in both habitats was spatially structured, with E. cunninghami showing high pairwise relatedness within their rocky retreat sites. Analysis of relatedness over different spatial scales, spatial autocorrelation of alleles and assignment tests, all indicated that both sexes in the cleared area show less dispersal than their counterparts in the reserve. Furthermore, deforestation may inhibit female dispersal to a greater extent than that of males. The geographical structuring of allele frequencies for adults in the cleared area, but not the reserve, indicates that habitat fragmentation has the potential to alter at least the microevolution of E. cunninghami populations.

Inbreeding avoidance in cunningham's skinks (Egernia cunninghami) in natural and fragmented habitat.

Habitat fragmentation/alteration has been proposed as a distinct process threatening the viability of populations of many organisms. One expression of its impact may be the disruption of core population processes such as inbreeding avoidance. Using the experimental design outlined in our companion paper, we report on the impact of habitat alteration (deforestation) on inbreeding in the rock‐dwelling Australian lizard Egernia cunninghami. Ten microsatellite loci were used to calculate relatedness coefficients of potential and actual breeding pairs, and to examine mate‐choice and heterozygosity. Despite significantly less dispersal and higher within‐group relatedness between potential mates in deforested than in natural habitats, this did not result in significantly more inbred matings. Average relatedness amongst breeding pairs was low, with no significant difference between natural and fragmented populations in relatedness between breeding pairs, or individual heterozygosity. Active avoidance of close kin as mates was indicated by the substantially and significantly lower relatedness in actual breeding pairs than potential ones. These facts, and heterozygote excesses in all groups of immature lizards from both habitats, show that E. cunninghami maintained outbreeding in the face of increased accumulation of relatives.

Antimicrobial defences increase with sociality in bees

Evidence for the antiquity and importance of microbial pathogens as selective agents is found in the proliferation of antimicrobial defences throughout the animal kingdom. Social insects, typified by crowding and often by low genetic variation, have high probabilities of disease transmission and eusocial Hymenoptera may be particularly vulnerable because of haplodiploidy. Mechanisms they employ to reduce the risk of disease include antimicrobial secretions which are particularly important primary barriers to infection. However, until now, whether or not there is selection for stronger antimicrobial secretions when the risk of disease increases because of sociality has not been tested. Here, we present evidence that the production of progressively stronger antimicrobial compounds was critical to the evolution of sociality in bees. We found that increases in group size and genetic relatedness were strongly correlated with increasing antimicrobial strength. The antimicrobials of even the most primitive semi-social species were an order of magnitude stronger that those of solitary species, suggesting a point of no return, beyond which disease control was essential. Our results suggest that selection by microbial pathogens was critical to the evolution of sociality and required the production of strong, front-line antimicrobial defences.

Nuclear and mitochondrial DNA reveals isolation of imperilled grey nurse shark populations (Carcharias taurus)

Loss of sharks and other upper‐trophic marine predators has sparked worldwide concern for the stability of ocean ecosystems. The grey nurse (ragged‐tooth or sand tiger) shark (Carcharias taurus) is Vulnerable on a global scale, Critically Endangered in Australia and presumed extinct in parts of its historical range. We used 193 muscle and fin samples collected from six extant populations to assess global mtDNA and microsatellite diversity and the degree of global population genetic structure. Control region mtDNA diversity was low in every population, and two populations (eastern Australia and Japan) contained only a single mtDNA haplotype. Genetic signatures of recent losses of genetic variation were not yet apparent at microsatellite loci, indicating that this low mtDNA variation is not a result of anthropogenic population declines. Population differentiation was substantial between each population pair except Brazil and South Africa, FST values ranged from 0.050 to 0.699 and 0.100 to 1.00 for microsatellite and mitochondrial data respectively. Bayesian analysis clearly partitioned individuals into five of the populations from which they were sampled. Our data imply a low frequency of immigrant exchange among each of these regions and we suggest that each be recognized as a distinct evolutionary significant unit. In contrast to pelagic species such as whale shark and white shark that may cross ocean basins and where cooperative international efforts are necessary for conservation, grey nurse shark, like many coastal species, need to be managed regionally.

High mate and site fidelity in Cunningham's skinks (Egernia cunninghami) in natural and fragmented habitat

While habitat alteration has considerable potential to disrupt important within‐population processes, such as mating and kin structure, via changed patterns of dispersal, this has rarely been tested. We are investigating the impact of anthropogenic habitat alteration on the population biology of the rock‐dwelling Australian lizard Egernia cunninghami on the Central Tablelands of New South Wales, Australia, by comparing deforested and adjacent naturally vegetated areas. The novel analyses in this paper, and its companion, build on previous work by adding a new replicate site, more loci and more individuals. The additional microsatellite loci yield sufficient power for parentage analysis and the sociobiological inferences that flow from it. Genetic and capture–mark–recapture techniques were used to investigate mate and site fidelity and associated kin structure. Analyses of the mating system and philopatry using 10 microsatellite loci showed high levels of site fidelity by parents and their offspring in natural and deforested habitats. Parentage assignment revealed few individuals with multiple breeding partners within seasons and fidelity of pairs across two or more breeding seasons was typical. Despite reduced dispersal, increased group sizes and significant, dramatic increases in relatedness among individuals within rock outcrops in deforested areas, no significant differences between deforested and natural areas were evident in the degree of multiple mating or philopatry of breeding partners within and across seasons. With the exception that there was a significantly higher proportion of unmated males in the deforested area, the social and mating structure of this species has so far been surprisingly robust to substantial perturbation of dispersal and relatedness structure. Nonetheless, approximately 10‐fold elevation of mean pairwise relatedness in the deforested areas has great potential to increase inbred matings, which is investigated in the companion paper.

Isolation and genetic diversity of endangered grey nurse shark (Carcharias taurus) populations

Anthropogenic impacts are believed to be the primary threats to the eastern Australian population of grey nurse sharks (Carcharias taurus), which is listed as critically endangered, and the most threatened population globally. Analyses of 235 polymorphic amplified fragment length polymorphisms (AFLP) loci and 700 base pairs of mitochondrial DNA control region provide the first account of genetic variation and geographical partitioning (east and west coasts of Australia, South Africa) in C. taurus. Assignment tests, analysis of relatedness and Fst values all indicate that the Australian populations are isolated from South Africa, with negligible migration between the east and west Australian coasts. There are significant differences in levels of genetic variation among regions. Australian C. taurus, particularly the eastern population, has significantly less AFLP variation than the other sampling localities. Further, the eastern Australian sharks possess only a single mitochondrial haplotype, also suggesting a small number of founding individuals. Therefore, historical, rather than anthropogenic processes most likely account for their depauperate genetic variation. These findings have implications for the viability of the eastern Australian population of grey nurse sharks.

Population structure of adult female Australian sea lions is driven by fine-scale foraging site fidelity

The Australian sea lion, Neophoca cinerea, one of the world’s rarest otariids, is notable for an asynchronous, aseasonal breeding chronology. Determining the ecological features that shape the genetic structure of marine predators such as Australian sea lions is challenging because their demersal foraging habitat is difficult to observe and quantify. Recent developments in stable isotope screening techniques using milk-dependent pups as proxies for maternal isotope signatures identified temporally stable, alternative (inshore and offshore) foraging ecotypes in adult female Australian sea lions. We combined this technique with mitochondrial DNA (mtDNA) analysis of samples of 40–60% of all pups produced at 17 of the largest South Australian colonies to determine whether ecological specialization in foraging ecotype within and between colonies has shaped maternal population structure within the species. Genetic isolation by distance was apparent at very fine geographical scales with three distinct clusters of colonies that share multiple haplotypes being interspersed with isolated breeding sites. There was no congruence between mtDNA haplotype distribution and foraging ecotypes suggesting that observed behavioural specialization was not maintained along matrilines. We propose that foraging specialization within discrete fine-scale foraging areas and habitats at the individual level limits the dispersive capacity of adult female Australian sea lions which in turn drives population structure. Given this species’ vulnerability to anthropogenic impacts and the high degree of female population structure, determining the extent of male-mediated gene flow in this species is critical. Only then can breeding colony connectivity be established and appropriate management units identified for the species.

Chemical and genetic defenses against disease in insect societies

The colonies of ants, bees, wasps and termites, the social insects, consist of large numbers of closely related individuals; circumstances ideal for contagious diseases. Antimicrobial assays of these animals have demonstrated a wide variety of chemical defenses against both bacteria and fungi that can be broadly classified as either external antiseptic compounds or internal immune molecules. Reducing the disease risks inherent in colonies of social insects is also achieved by behaviors, such as multiple mating or dispersal, that lower genetic relatedness both within- and among colonies. The interactions between social insects and their pathogens are complex, as illustrated by some ants that require antimicrobial and behavioral defenses against highly specialized fungi, such as those in the genus Cordyceps that attack larvae and adults and species in the genus Escovopsis that attack their food supplies. Studies of these defenses, especially in ants, have revealed remarkably sophisticated immune systems, including peptides induced by, and specific to, individual bacterial strains. The latter may be the result of the recruitment by the ants of antibiotic-producing bacteria but the extent of such three-way interactions remains unknown. There is strong experimental evidence that the evolution of sociality required dramatic increases in antimicrobial defenses and that microbes have been powerful selective agents. The antimicrobial chemicals and the insect-killing fungi may be useful in medicine and agriculture, respectively.

Lizards Cooperatively Tunnel to Construct a Long-Term Home for Family Members

Constructing a home to protect offspring while they mature is common in many vertebrate groups, but has not previously been reported in lizards. Here we provide the first example of a lizard that constructs a long-term home for family members, and a rare case of lizards behaving cooperatively. The great desert skink, Liopholis kintorei from Central Australia, constructs an elaborate multi-tunnelled burrow that can be continuously occupied for up to 7 years. Multiple generations participate in construction and maintenance of burrows. Parental assignments based on DNA analysis show that immature individuals within the same burrow were mostly full siblings, even when several age cohorts were present. Parents were always captured at burrows containing their offspring, and females were only detected breeding with the same male both within- and across seasons. Consequently, the individual investments made to construct or maintain a burrow system benefit their own offspring, or siblings, over several breeding seasons.

Rapid isolation of the first set of polymorphic microsatellite loci from the Australian gummy shark, Mustelus antarcticus and their utility across divergent shark taxa

The development of genetic markers for studies of population structure and genetic diversity can be applied to improving management and monitoring of commercially fished species. Here we report on the use of high-throughput (454) sequencing to develop a panel of 12 novel polymorphic microsatellite markers for the commercially harvested gummy shark, Mustelus antarcticus. This constitutes the first suite of microsatellites developed for the genus Mustelus, a group which features in commercial fisheries around the world. We demonstrate the successful amplification of these markers in other species of Mustelus and test their utility in species from an additional nine genera of shark.