Lee Ann Rollins

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.

Females use multiple mating and genetically loaded sperm competition to target compatible genes

Sauce for the Goose? Extra-pair copulations benefit males by increasing their potential number of offspring. However, whether they have adaptive significance for females has long been debated. Pryke et al. (p. 964), provided female finches four different scenarios to test when extra-pair copulations occurred and measured the paternity of the resulting offspring. By varying the potential fathers from a supposedly adaptive, compatible male through a neutral context, to a supposedly maladaptive scenario, females biased paternity to the extra-pair male when his contribution was adaptive and away from the extra-pair male when his contribution was maladaptive. Thus, despite bias in copulation frequency in favor of the social pair, cryptic female choice may show a fertilization bias toward compatible genes. Female birds that have multiple mates favor fertilization by the most genetically compatible father. Individuals in socially monogamous species may participate in copulations outside of the pair bond, resulting in extra-pair offspring. Although males benefit from such extra-pair behavior if they produce more offspring, the adaptive function of infidelity to females remains elusive. Here we show that female participation in extra-pair copulations, combined with a genetically loaded process of sperm competition, enables female finches to target genes that are optimally compatible with their own to ensure fertility and optimize offspring viability. Such female behavior, along with the postcopulatory processes demonstrated here, may provide an adaptive function of female infidelity in socially monogamous animals.

Building genetic networks using relatedness information: a novel approach for the estimation of dispersal and characterization of group structure in social animals

Natal dispersal is an important life history trait driving variation in individual fitness, and therefore, a proper understanding of the factors underlying dispersal behaviour is critical to many fields including population dynamics, behavioural ecology and conservation biology. However, individual dispersal patterns remain difficult to quantify despite many years of research using direct and indirect methods. Here, we quantify dispersal in a single intensively studied population of the cooperatively breeding chestnut‐crowned babbler (Pomatostomus ruficeps) using genetic networks created from the combination of pairwise relatedness data and social networking methods and compare this to dispersal estimates from re‐sighting data. This novel approach not only identifies movements between social groups within our study sites but also provides an estimation of immigration rates of individuals originating outside the study site. Both genetic and re‐sighting data indicated that dispersal was strongly female biased, but the magnitude of dispersal estimates was much greater using genetic data. This suggests that many previous studies relying on mark–recapture data may have significantly underestimated dispersal. An analysis of spatial genetic structure within the sampled population also supports the idea that females are more dispersive, with females having no structure beyond the bounds of their own social group, while male genetic structure expands for 750 m from their social group. Although the genetic network approach we have used is an excellent tool for visualizing the social and genetic microstructure of social animals and identifying dispersers, our results also indicate the importance of applying them in parallel with behavioural and life history data.

Population genetic tools for pest management: a review.

Population genetic tools have the potential to answer key questions in pest management including quantifying the number of genetically distinct populations represented in an invasion, the number of individuals present, whether populations are expanding or contracting, identifying the origin of invasive individuals, the number of separate introduction events that have occurred and in which order, and the rate that individuals are moving between populations. Genetic methods have only recently gained sufficient resolution to address these questions due to advances in laboratory techniques coupled with an increase in computational power. In combination, these methods may lead to a more comprehensive understanding of the dynamics of invasions. The expansion of the European starling (Sturnus vulgaris) into Western Australia is used as an applied example of how genetic methods can be integrated to provide vital information to improve pest-management strategies. Invasion events also may provide a unique opportunity to test some of these methodologies.

A genetic perspective on rapid evolution in cane toads (Rhinella marina)

The process of biological invasion exposes a species to novel pressures, in terms of both the environments it encounters and the evolutionary consequences of range expansion. Several invaders have been shown to exhibit rapid evolutionary changes in response to those pressures, thus providing robust opportunities to clarify the processes at work during rapid phenotypic transitions. The accelerating pace of invasion of cane toads (Rhinella marina) in tropical Australia during its 80‐year history has been well characterized at the phenotypic level, including common‐garden experiments that demonstrate heritability of several dispersal‐relevant traits. Individuals from the invasion front (and their progeny) show distinctive changes in morphology, physiology and behaviour that, in combination, result in far more rapid dispersal than is true of conspecifics from long‐colonized areas. The extensive body of work on cane toad ecology enables us to place into context studies of the genetic basis of these traits. Our analyses of differential gene expression from toads from both ends of this invasion‐history transect reveal substantial upregulation of many genes, notably those involved in metabolism and cellular repair. Clearly, then, the dramatically rapid phenotypic evolution of cane toads in Australia has been accompanied by substantial shifts in gene expression, suggesting that this system is well suited to investigating the genetic underpinnings of invasiveness.

Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird

Kin selection theory has been the central model for understanding the evolution of cooperative breeding, where non-breeders help bear the cost of rearing young. Recently, the dominance of this idea has been questioned; particularly in obligate cooperative breeders where breeding without help is uncommon and seldom successful. In such systems, the direct benefits gained through augmenting current group size have been hypothesized to provide a tractable alternative (or addition) to kin selection. However, clear empirical tests of the opposing predictions are lacking. Here, we provide convincing evidence to suggest that kin selection and not group augmentation accounts for decisions of whether, where and how often to help in an obligate cooperative breeder, the chestnut-crowned babbler (Pomatostomus ruficeps). We found no evidence that group members base helping decisions on the size of breeding units available in their social group, despite both correlational and experimental data showing substantial variation in the degree to which helpers affect productivity in units of different size. By contrast, 98 per cent of group members with kin present helped, 100 per cent directed their care towards the most related brood in the social group, and those rearing half/full-sibs helped approximately three times harder than those rearing less/non-related broods. We conclude that kin selection plays a central role in the maintenance of cooperative breeding in this species, despite the apparent importance of living in large groups.

High genetic diversity is not essential for successful introduction

Some introduced populations thrive and evolve despite the presumed loss of diversity at introduction. We aimed to quantify the amount of genetic diversity retained at introduction in species that have shown evidence of adaptation to their introduced environments. Samples were taken from native and introduced ranges of Arctotheca populifolia and Petrorhagia nanteuilii. Using microsatellite data, we identified the source for each introduction, estimated genetic diversity in native and introduced populations, and calculated the amount of diversity retained in introduced populations. These values were compared to those from a literature review of diversity in native, confamilial populations and to estimates of genetic diversity retained at introduction. Gene diversity in the native range of both species was significantly lower than for confamilials. We found that, on average, introduced populations showing evidence of adaptation to their new environments retained 81% of the genetic diversity from the native range. Introduced populations of P. nanteuilii had higher genetic diversity than found in the native source populations, whereas introduced populations of A. populifolia retained only 14% of its native diversity in one introduction and 1% in another. Our literature review has shown that most introductions demonstrating adaptive ability have lost diversity upon introduction. The two species studied here had exceptionally low native range genetic diversity. Further, the two introductions of A. populifolia represent the largest percentage loss of genetic diversity in a species showing evidence of substantial morphological change in the introduced range. While high genetic diversity may increase the likelihood of invasion success, the species examined here adapted to their new environments with very little neutral genetic diversity. This finding suggests that even introductions founded by small numbers of individuals have the potential to become invasive.

Parental care in wild and captive zebra finches : measuring food delivery to quantify parental effort

Although the zebra finch, Taeniopygia guttata, has been a very important model system for the study of intrafamilial conflict and parental strategies, a detailed understanding of the variation in parental effort that can occur both within and between pairs is lacking. In part this is because many different methods have been used by individual studies to quantify parental care (i.e. nest visit rate, time in the nest and number of feeds per visit), but these have not directly been compared. We used nestbox cameras to monitor parental visit rate and the distribution of food among the nestlings in domestic, captive wild and wild free-living zebra finches. The percentage of nest visits by parents in which they fed the nestlings was consistent, with multiple feeds to different nestlings occurring within a single visit. The quantity of food delivered and its distribution among the nestlings, however, varied greatly both within and between broods. The number of regurgitations a brood received correlated significantly with the number of individual feeds when accounting for environment, but not with nest visit rate or the duration of time parents spent in the nestbox. In captive conditions, parents visited the nest at twice the rate of wild free-living birds, overall providing nestlings with twice the amount of food. Captive conditions also led to food distribution becoming less equitable among the brood, owing to changes in the number of regurgitations per individual feed and the number of overall feeds per nest visit.

Mothers adjust offspring sex to match the quality of the rearing environment

Theory predicts that mothers should adjust offspring sex ratios when the expected fitness gains or rearing costs differ between sons and daughters. Recent empirical work has linked biased offspring sex ratios to environmental quality via changes in relative maternal condition. It is unclear, however, whether females can manipulate offspring sex ratios in response to environmental quality alone (i.e. independent of maternal condition). We used a balanced within-female experimental design (i.e. females bred on both low- and high-quality diets) to show that female parrot finches (Erythrura trichroa) manipulate primary offspring sex ratios to the quality of the rearing environment, and not to their own body condition and health. Individual females produced an unbiased sex ratio on high-quality diets, but over-produced sons in poor dietary conditions, even though they maintained similar condition between diet treatments. Despite the lack of sexual size dimorphism, such sex ratio adjustment is in line with predictions from sex allocation theory because nutritionally stressed foster sons were healthier, grew faster and were more likely to survive than daughters. These findings suggest that mothers may adaptively adjust offspring sex ratios to optimally match their offspring to the expected quality of the rearing environment.

SEX‐DEPENDENT SELECTION DIFFERENTIALLY SHAPES GENETIC VARIATION ON AND OFF THE GUPPY Y CHROMOSOME

Because selection is often sex‐dependent, alleles can have positive effects on fitness in one sex and negative effects in the other, resulting in intralocus sexual conflict. Evolutionary theory predicts that intralocus sexual conflict can drive the evolution of sex limitation, sex‐linkage, and sex chromosome differentiation. However, evidence that sex‐dependent selection results in sex‐linkage is limited. Here, we formally partition the contribution of Y‐linked and non‐Y‐linked quantitative genetic variation in coloration, tail, and body size of male guppies (Poecilia reticulata)—traits previously implicated as sexually antagonistic. We show that these traits are strongly genetically correlated, both on and off the Y chromosome, but that these correlations differ in sign and magnitude between both parts of the genome. As predicted, variation in attractiveness was found to be associated with the Y‐linked, rather than with the non‐Y‐linked component of genetic variation in male ornamentation. These findings show how the evolution of Y‐linkage may be able to resolve sexual conflict. More generally, they provide unique insight into how sex‐specific selection has the potential to differentially shape the genetic architecture of fitness traits across different parts of the genome.