William B. Sherwin

Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change

It is important to detect population bottlenecks in threatened and managed species because bottlenecks can increase the risk of population extinction. Early detection is critical and can be facilitated by statistically powerful monitoring programs for detecting bottleneck‐induced genetic change. We used Monte Carlo computer simulations to evaluate the power of the following tests for detecting genetic changes caused by a severe reduction in a populations effective size (Ne): a test for loss of heterozygosity, two tests for loss of alleles, two tests for change in the distribution of allele frequencies, and a test for small Ne based on variance in allele frequencies (the ‘variance test’). The variance test was most powerful; it provided an 85% probability of detecting a bottleneck of size Ne = 10 when monitoring five microsatellite loci and sampling 30 individuals both before and one generation after the bottleneck. The variance test was almost 10‐times more powerful than a commonly used test for loss of heterozygosity, and it allowed for detection of bottlenecks before 5% of a populations heterozygosity had been lost. The second most powerful tests were generally the tests for loss of alleles. However, these tests had reduced power for detecting genetic bottlenecks caused by skewed sex ratios. We provide guidelines for the number of loci and individuals needed to achieve high‐power tests when monitoring via the variance test. We also illustrate how the variance test performs when monitoring loci that have widely different allele frequency distributions as observed in five wild populations of mountain sheep (Ovis canadensis).

Genetic variation of microsatellite loci in a bottlenecked species: the northern hairy-nosed wombat Lasiorhinus krefftii.

We investigate the utility of hypervariable microsatellite loci to measure genetic variability remaining in the northern hairy‐nosed wombat, one of Australias rarest mammals. This species suffered a dramatic range and population reduction over the past 120 years and now exists as a single colony of about 70 individuals at Epping Forest National Park, central Queensland. Because our preliminary research on mitochondrial DNA and multilocus DNA fingerprints did not reveal informative variation in this population, we chose to examine variation in microsatellite repeats, a class of loci known to be highly polymorphic in mammals. To assess the suitability of various wombat populations as a reference for comparisons of genetic variability and subdivision we further analysed mitochondrial DNA cytochrome b sequence, using phylogenetic methods. Our results show that appreciable levels of variation still exist in the Epping Forest colony although it has only 41% of the heterozygosity shown in a population of a closely‐related species. From museum specimens collected in 1884, we also assessed microsatellite variation in an extinct population of the northern hairy‐nosed wombat, from Deniliquin, New South Wales, 2000 km to the south of the extant population. The apparent loss of variation in the Epping Forest colony is consistent with an extremely small effective population size throughout its 120‐year decline.

Low genetic variability of the koala Phascolarctos cinereus in south‐eastern Australia following a severe population bottleneck

Genotyping of koalas at CA‐repeat microsatellite loci has revealed significant differences in the levels of allelic diversity (A) and expected heterozygosity (HE) between populations from north‐eastern and south‐eastern Australia. In the 10 populations studied, allelic diversity ranged from 8.0 in the Nowendoc population to 1.7 in the Kangaroo Is. population, and values of HE ranged from 0.831 in the Nowendoc population to 0.331 in the Kangaroo Is. population. Data from pooled populations revealed koalas from the northeastern region had significantly higher levels of allelic diversity (A= 11.5 ± 1.4) than those from south‐eastern Australia (A= 5.3 ± 1.0). Furthermore significantly higher heterozygosity levels were found in the north‐eastern (HE= 0.851) vs. the south‐eastern (HE= 0.436) regions of Australia. Following a near‐extinction bottleneck in the 1920s, mainland Victorian and Kangaroo Is. koalas have been involved in an extensive program of relocations. The source populations of the relocated animals were islands in Westernport Bay, which were founded by very few individuals in the late 1800s and early 1900s. The significantly lower levels of variation between south‐eastern Australian populations suggests that human intervention has had a severe effect on levels of genetic diversity in this region, and this may have long‐term genetic consequences.

Social and genetic interactions drive fitness variation in a free-living dolphin population

The evolutionary forces that drive fitness variation in species are of considerable interest. Despite this, the relative importance and interactions of genetic and social factors involved in the evolution of fitness traits in wild mammalian populations are largely unknown. To date, a few studies have demonstrated that fitness might be influenced by either social factors or genes in natural populations, but none have explored how the combined effect of social and genetic parameters might interact to influence fitness. Drawing from a long-term study of wild bottlenose dolphins in the eastern gulf of Shark Bay, Western Australia, we present a unique approach to understanding these interactions. Our study shows that female calving success depends on both genetic inheritance and social bonds. Moreover, we demonstrate that interactions between social and genetic factors also influence female fitness. Therefore, our study represents a major methodological advance, and provides critical insights into the interplay of genetic and social parameters of fitness.

Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies

Male bottlenose dolphins (Tursiops sp.) in Shark Bay have one of the most complex male societies outside humans. Two broad mating strategies have been identified in males. In the first strategy, there are two types of alliances: stable‘first–order’ pairs and trios that herd individual females in reproductive condition, and ‘second–order’ teams of two first–order alliances (five or six individuals) that join forces against rivals in contests for females. In the alternative strategy, a ‘super–alliance’ of ca. 14 individuals, males form pairs or trios to herd females, but in contrast to the stable alliances, these pairs and trios are highly labile. Here, we show that males in stable first–order alliances and the derived second–order alliances are often strongly related, so that they may gain inclusive fitness benefits from alliance membership. By contrast, members of the super–alliance are no more closely related than expected by chance. Further, the strength of the association of alliance partners within the super–alliance, as measured by an index of joint participation in consorting a female, was not correlated with their genetic relatedness. Thus, within one population and one sex, it appears that there may be simultaneous operation of more than one mode of group formation.

'O father: where art thou?'--Paternity assessment in an open fission-fusion society of wild bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia.

Sexually mature male bottlenose dolphins in Shark Bay cooperate by pursuing distinct alliance strategies to monopolize females in reproductive condition. We present the results of a comprehensive study in a wild cetacean population to test whether male alliance membership is a prerequisite for reproductive success. We compared two methods for inferring paternity: both calculate a likelihood ratio, called the paternity index, between two opposing hypotheses, but they differ in the way that significance is applied to the data. The first method, a Bayesian approach commonly used in human paternity testing, appeared to be overly conservative for our data set, but would be less susceptible to assumptions if a larger number of microsatellite loci had been used. Using the second approach, the computer program cervus 2.0, we successfully assigned 11 paternities to nine males, and 17 paternities to 14 out of 139 sexually mature males at 95% and 80% confidence levels, respectively. It appears that being a member of a bottlenose dolphin alliance is not a prerequisite for paternity: two paternities were obtained by juvenile males (one at the 95%, the other at the 80% confidence level), suggesting that young males without alliance partners pursue different mating tactics to adults. Likelihood analyses showed that these two juvenile males were significantly more likely to be the true father of the offspring than to be their half‐sibling (P < 0.05). Using paternity data at an 80% confidence level, we could show that reproductive success was significantly skewed within at least some stable first‐order alliances (P < 0.01). Interestingly, there is powerful evidence that one mating was incestuous, with one calf apparently fathered by its mothers father (P < 0.01). Our study suggests that the reproductive success of both allied males, and of nonallied juveniles, needs to be incorporated into an adaptive framework that seeks to explain alliance formation in male bottlenose dolphins.

Invasive species can't cover their tracks : using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia

Invasive species are known to cause environmental and economic damage, requiring management by control agencies worldwide. These species often become well established in new environments long before their detection, resulting in a lack of knowledge regarding their history and dynamics. When new invasions are discovered, information regarding the source and pathway of the invasion, and the degree of connectivity with other populations can greatly benefit management strategies. Here we use invasive common starling (Sturnus vulgaris) populations from Australia to demonstrate that genetic techniques can provide this information to aid management, even when applied to highly vagile species over continental scales. Analysis of data from 11 microsatellites in 662 individuals sampled at 17 localities across their introduced range in Australia revealed four populations. One population consisted of all sampling sites from the expansion front in Western Australia, where control efforts are focused. Despite evidence of genetic exchange over both contemporary and historical timescales, gene flow is low between this population and all three more easterly populations. This suggests that localized control of starlings on the expansion front may be an achievable goal and the long‐standing practice of targeting select proximal eastern source populations may be ineffective on its own. However, even with low levels of gene flow, successful control of starlings on the expansion front will require vigilance, and genetic monitoring of this population can provide essential information to managers. The techniques used here are broadly applicable to invasive populations worldwide.

Measurement of biological information with applications from genes to landscapes

Biological diversity is quantified for reasons ranging from primer design, to bioprospecting, and community ecology. As a common index for all levels, we suggest Shannons SH, already used in information theory and biodiversity of ecological communities. Since Lewontins first use of this index to describe human genetic variation, it has been used for variation of viruses, splice‐junctions, and informativeness of pedigrees. However, until now there has been no theory to predict expected values of this index under given genetic and demographic conditions. We present a new null theory for SH at the genetic level, and show that this index has advantages including (i) independence of measures at each hierarchical level of organization; (ii) robust estimation of genetic exchange over a wide range of conditions; (iii) ability to incorporate information on population size; and (iv) explicit relationship to standard statistical tests. Utilization of this index in conjunction with other existing indices offers powerful insights into genetic processes. Our genetic theory is also extendible to the ecological community level, and thus can aid the comparison and integration of diversity at the genetic and community levels, including the need for measures of community diversity that incorporate the genetic differentiation between species.

Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins

Few studies of kinship in mammalian societies have been able to consider the complex interactions between home range overlap, association patterns and kinship, which have created a critical gap in our understanding of social evolution. We investigated the association patterns of female bottlenose dolphins, Tursiops aduncus, in the eastern gulf of Shark Bay, Western Australia and found that they depended upon the complex interplay of at least three factors: home range overlap, matrilineal kinship and biparental kinship. While home range overlap was positively correlated with female association patterns, preferred associations were found between females showing as little as 27% home range overlap, and some pairs showed avoidance despite 100% home range overlap. Furthermore, on average, both casual and preferred associations took place between females that were more closely biparentally related than expected by chance and this pattern varied depending upon whether or not pairs of females shared the same matriline.

Phylogeographical population structure of tiger quolls Dasyurus maculatus (Dasyuridae: Marsupialia), an endangered carnivorous marsupial

Tiger quolls, Dasyurus maculatus, are the largest carnivorous marsupials still extant on the mainland of Australia, and occupy an important ecological niche as top predators and scavengers. Two allopatric subspecies are recognized, D.m. gracilis in north Queensland, and D.m. maculatus in the southeast of the mainland and Tasmania. D.m. gracilis is considered endangered while D.m. maculatus is listed as vulnerable to extinction; both subspecies are still in decline. Phylogeographical subdivision was examined to determine evolutionarily significant units (ESUs) and management units (MUs) among populations of tiger quolls to assist in the conservation of these taxa. Ninety‐three tiger quolls from nine representative populations were sampled from throughout the species range. Six nuclear microsatellite loci and the mitochondrial DNA (mtDNA) control region (471 bp) were used to examine ESUs and MUs in this species. We demonstrated that Tasmanian tiger quolls are reciprocally monophyletic to those from the mainland using mtDNA analysis, but D.m. gracilis was not monophyletic with respect to mainland D.m. maculatus. Analysis of microsatellite loci also revealed significant differences between the Tasmanian and mainland tiger quolls, and between D.m. gracilis and mainland D.m. maculatus. These results indicate that Tasmanian and mainland tiger quolls form two distinct evolutionary units but that D.m. gracilis and mainland D.m. maculatus are different MUs within the same ESU. The two marker types used in this study revealed different male and female dispersal patterns and indicate that the most appropriate units for short‐term management are local populations. A revised classification and management plan are needed for tiger quolls, particularly in relation to conservation of the Tasmanian and Queensland populations.