Global terrestrial invasions: Where naturalised birds, mammals, and plants might spread next and what affects this process.

More species live outside their native range than at any point in human history. Yet, there is little understanding of the geographic regions that will be threatened if these species continue to spread, nor of whether they will spread. We predict the world's terrestrial regions to which 833 naturalised plants, birds, and mammals are most imminently likely to spread, and investigate what factors have hastened or slowed their spread to date. There is huge potential for further spread of naturalised birds in North America, mammals in Eastern Europe, and plants in North America, Eastern Europe, and Australia. Introduction history, dispersal, and the spatial distribution of suitable areas are more important predictors of species spread than traits corresponding to habitat usage or biotic interactions. Natural dispersal has driven spread in birds more than in plants. Whether these taxa continue to spread more widely depends partially on connectivity of suitable environments. Plants show the clearest invasion lag, and the putative importance of human transportation indicates opportunities to slow their spread. Despite strong predictive effects, questions remain, particularly why so many birds in North America do not occupy climatically suitable areas close to their existing ranges.

Multi-locus homozygosity promotes actuarial senescence in a wild mammal.

Genome-wide homozygosity, caused for example by inbreeding, is expected to have deleterious effects on survival and/or reproduction. Evolutionary theory predicts that any fitness costs are likely to be detected in late life because natural selection will filter out negative impacts on younger individuals with greater reproductive value. Here we infer associations between multi-locus homozygosity (MLH), sex, disease and age-dependent mortality risks using Bayesian analysis of the life histories of wild European badgers Meles meles in a population naturally infected with Mycobacterium bovis (the causative agent of bovine tuberculosis [bTB]). We find important effects of MLH on all parameters of the Gompertz-Makeham mortality hazard function, but particularly in later life. Our findings confirm the predicted association between genomic homozygosity and actuarial senescence. Increased homozygosity is particularly associated with an earlier onset, and greater rates of actuarial senescence, regardless of sex. The association between homozygosity and actuarial senescence is further amplified among badgers putatively infected with bTB. These results recommend further investigation into the ecological and behavioural processes that result in genome-wide homozygosity, and focused work on whether homozygosity is harmful or beneficial during early life-stages.

Stress causes interspecific facilitation within a compost community.

Ecological theory predicts interactions between species to become more positive under abiotic stress, while competition should prevail in more benign environments. However, experimental tests of this stress gradient hypothesis in natural microbial communities are lacking. We test this hypothesis by measuring interactions between 10 different members of a bacterial community inhabiting potting compost in the presence or absence of toxic copper stress. We found that copper stress caused significant net changes in species interaction signs, shifting the net balance towards more positive interactions. This pattern was at least in part driven by copper-sensitive isolates - that produced relatively small amounts of metal-detoxifying siderophores - benefitting from the presence of other species that produce extracellular detoxifying agents. As well as providing support for the stress gradient hypothesis, our results highlight the importance of community-wide public goods in shaping microbial community composition.

Ecological selection of siderophore-producing microbial taxa in response to heavy metal contamination.

Some microbial public goods can provide both individual and community-wide benefits, and are open to exploitation by non-producing species. One such example is the production of metal-detoxifying siderophores. Here, we investigate whether conflicting selection pressures on siderophore production by heavy metals - a detoxifying effect of siderophores, and exploitation of this detoxifying effect - result in a net increase or decrease. We show that the proportion of siderophore-producing taxa increases along a natural heavy metal gradient. A causal link between metal contamination and siderophore production was subsequently demonstrated in a microcosm experiment in compost, in which we observed changes in community composition towards taxa that produce relatively more siderophores following copper contamination. We confirmed the selective benefit of siderophores by showing that taxa producing large amounts of siderophore suffered less growth inhibition in toxic copper. Our results suggest that ecological selection will favour siderophore-mediated decontamination, with important consequences for potential remediation strategies.

Inbreeding intensifies sex- and age-dependent disease in a wild mammal.

The mutation accumulation theory of senescence predicts that age-related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and progression of disease. Evidence is growing for natural links between inbreeding and ageing; between inbreeding and disease; between sex and ageing; and between sex and disease. However, there is scant evidence, to date, for links among age, disease, inbreeding and sex in a single natural population. Using ecological and epidemiological data from a long-term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis (bTB), inbreeding (measured as multilocus homozygosity) intensifies a positive correlation between age and evidence of progressed infection (measured as an antibody response to bTB), but only among females. Male badgers suffer a steeper relationship between age and progressed infection than females, with no influence of inbred status. We found no link between inbreeding and the incidence of progressed infection during early life in either sex. Our findings highlight an age-related increase in the impact of inbreeding on a fitness-relevant trait (disease state) among females. This relationship is consistent with the predictions of the mutation accumulation theory of senescence, but other mechanisms could also play a role. For example, late-life declines in condition, arising through mechanisms other than mutation accumulation might have increased the magnitude of inbreeding depression in late life. Whichever mechanism causes the observed patterns, we have shown that inbreeding can influence age-dependent patterns of disease and, by extension, is likely to affect the magnitude and timing of the late-life declines in components of fitness that characterise senescence. Better understanding of sex-specific links between inbreeding, disease and ageing provides insights into population-level pathogen dynamics and could influence management strategies for wildlife reservoirs of zoonotic disease.

Demographic buffering and compensatory recruitment promotes the persistence of disease in a wildlife population.

Demographic buffering allows populations to persist by compensating for fluctuations in vital rates, including disease-induced mortality. Using long-term data on a badger (Meles meles Linnaeus, 1758) population naturally infected with Mycobacterium bovis, we built an integrated population model to quantify impacts of disease, density and environmental drivers on survival and recruitment. Badgers exhibit a slow life-history strategy, having high rates of adult survival with low variance, and low but variable rates of recruitment. Recruitment exhibited strong negative density-dependence, but was not influenced by disease, while adult survival was density independent but declined with increasing prevalence of diseased individuals. Given that reproductive success is not depressed by disease prevalence, density-dependent recruitment of cubs is likely to compensate for disease-induced mortality. This combination of slow life history and compensatory recruitment promotes the persistence of a naturally infected badger population and helps to explain the badger's role as a persistent reservoir of M. bovis.

Blood thicker than water: kinship, disease prevalence and group size drive divergent patterns of infection risk in a social mammal.

The importance of social- and kin-structuring of populations for the transmission of wildlife disease is widely assumed but poorly described. Social structure can help dilute risks of transmission for group members, and is relatively easy to measure, but kin-association represents a further level of population sub-structure that is harder to measure, particularly when association behaviours happen underground. Here, using epidemiological and molecular genetic data from a wild, high-density population of the European badger (Meles meles), we quantify the risks of infection with Mycobacterium bovis (the causative agent of tuberculosis) in cubs. The risk declines with increasing size of its social group, but this net dilution effect conceals divergent patterns of infection risk. Cubs only enjoy reduced risk when social groups have a higher proportion of test-negative individuals. Cubs suffer higher infection risk in social groups containing resident infectious adults, and these risks are exaggerated when cubs and infectious adults are closely related. We further identify key differences in infection risk associated with resident infectious males and females. We link our results to parent-offspring interactions and other kin-biased association, but also consider the possibility that susceptibility to infection is heritable. These patterns of infection risk help to explain the observation of a herd immunity effect in badgers following low-intensity vaccination campaigns. They also reveal kinship and kin-association to be important, and often hidden, drivers of disease transmission in social mammals.

Robust set-point regulation for ecological models with multiple management goals.

Population managers will often have to deal with problems of meeting multiple goals, for example, keeping at specific levels both the total population and population abundances in given stage-classes of a stratified population. In control engineering, such set-point regulation problems are commonly tackled using multi-input, multi-output proportional and integral (PI) feedback controllers. Building on our recent results for population management with single goals, we develop a PI control approach in a context of multi-objective population management. We show that robust set-point regulation is achieved by using a modified PI controller with saturation and anti-windup elements, both described in the paper, and illustrate the theory with examples. Our results apply more generally to linear control systems with positive state variables, including a class of infinite-dimensional systems, and thus have broader appeal.

Aphids Pick Their Poison: Selective Sequestration of Plant Chemicals Affects Host Plant Use in a Specialist Herbivore.

In some plant-insect interactions, specialist herbivores exploit the chemical defenses of their food plant to their own advantage. Brassica plants produce glucosinolates that are broken down into defensive toxins when tissue is damaged, but the specialist aphid, Brevicoryne brassicae, uses these chemicals against its own natural enemies by becoming a "walking mustard-oil bomb". Analysis of glucosinolate concentrations in plant tissue and associated aphid colonies reveals that not only do aphids sequester glucosinolates, but they do so selectively. Aphids specifically accumulate sinigrin to high concentrations while preferentially excreting a structurally similar glucosinolate, progoitrin. Surveys of aphid infestation in wild populations of Brassica oleracea show that this pattern of sequestration and excretion maps onto host plant use. The probability of aphid infestation decreases with increasing concentrations of progoitrin in plants. Brassica brassicae, therefore, appear to select among food plants according to plant secondary metabolite profiles, and selectively store only some compounds that are used against their own enemies. The results demonstrate chemical and behavioral mechanisms that help to explain evidence of geographic patterns and evolutionary dynamics in Brassica-aphid interactions.

Integral control for population management.

We present a novel management methodology for restocking a declining population. The strategy uses integral control, a concept ubiquitous in control theory which has not been applied to population dynamics. Integral control is based on dynamic feedback-using measurements of the population to inform management strategies and is robust to model uncertainty, an important consideration for ecological models. We demonstrate from first principles why such an approach to population management is suitable via theory and examples.

Mortality trajectory analysis reveals the drivers of sex-specific epidemiology in natural wildlife-disease interactions.

In animal populations, males are commonly more susceptible to disease-induced mortality than females. However, three competing mechanisms can cause this sex bias: weak males may simultaneously be more prone to exposure to infection and mortality; being 'male' may be an imperfect proxy for the underlying driver of disease-induced mortality; or males may experience increased severity of disease-induced effects compared with females. Here, we infer the drivers of sex-specific epidemiology by decomposing fixed mortality rates into mortality trajectories and comparing their parameters. We applied Bayesian survival trajectory analysis to a 22-year longitudinal study of a population of badgers (Meles meles) naturally infected with bovine tuberculosis (bTB). At the point of infection, infected male and female badgers had equal mortality risk, refuting the hypothesis that acquisition of infection occurs in males with coincidentally high mortality. Males and females exhibited similar levels of heterogeneity in mortality risk, refuting the hypothesis that maleness is only a proxy for disease susceptibility. Instead, sex differences were caused by a more rapid increase in male mortality rates following infection. Males are indeed more susceptible to bTB, probably due to immunological differences between the sexes. We recommend this mortality trajectory approach for the study of infection in animal populations.

Bounds on the dynamics of sink populations with noisy immigration.

Sink populations are doomed to decline to extinction in the absence of immigration. The dynamics of sink populations are not easily modelled using the standard framework of per capita rates of immigration, because numbers of immigrants are determined by extrinsic sources (for example, source populations, or population managers). Here we appeal to a systems and control framework to place upper and lower bounds on both the transient and future dynamics of sink populations that are subject to noisy immigration. Immigration has a number of interpretations and can fit a wide variety of models found in the literature. We apply the results to case studies derived from published models for Chinook salmon (Oncorhynchus tshawytscha) and blowout penstemon (Penstemon haydenii).

Life histories are not just fast or slow.

Life history strategies, which combine schedules of survival, development, and reproduction, shape how natural selection acts on species' heritable traits and organismal fitness. Comparative analyses have historically ranked life histories along a fast-slow continuum, describing a negative association between time allocation to reproduction and development versus survival. However, higher-quality, more representative data and analyses have revealed that life history variation cannot be fully accounted for by this single continuum. Moreover, studies often do not test predictions from existing theories and instead operate as exploratory exercises. To move forward, we offer three recommendations for future investigations: standardizing life history traits, overcoming taxonomic siloes, and using theory to move from describing to understanding life history variation across the Tree of Life.

Cat: Empirical modelling of Felis catus population dynamics in the UK.

Domestic cats are popular companion animals, however not all live in human homes and many cats live within shelters or as free-roaming, unowned- feral or stray cats. Cats can transition between these subpopulations, but the influence of this connectivity on overall population dynamics, and the effectiveness of management interventions, remain poorly understood. We developed a UK-focused multistate Matrix Population Model (MPM), combining multiple life history parameters into an integrated model of cat demography and population dynamics. The model characterises cats according to their age, subpopulation and reproductive status, resulting in a 28-state model. We account for density-dependence, seasonality and uncertainty in our modelled projections. Through simulations, we examine the model by testing the effect of different female owned-cat neutering scenarios over a 10-year projection timespan. We also use the model to identify the vital rates to which total population growth is most sensitive. The current model framework demonstrates that increased prevalence of neutering within the owned cat subpopulation influences the population dynamics of all subpopulations. Further simulations find that neutering owned cats younger is sufficient to reduce overall population growth rate, regardless of the overall neutering prevalence. Population growth rate is most influenced by owned cat survival and fecundity. Owned cats, which made up the majority of our modelled population, have the most influence on overall population dynamics, followed by stray, feral and then shelter cats. Due to the importance of owned-cat parameters within the current model framework, we find cat population dynamics are most sensitive to shifts in owned cat husbandry. Our results provide a first evaluation of the demography of the domestic cat population in the UK and provide the first structured population model of its kind, thus contributing to a wider understanding of the importance of modelling connectivity between subpopulations. Through example scenarios we highlight the importance of studying domestic cat populations in their entirety to better understand factors influencing their dynamics and to guide management planning. The model provides a theoretical framework for further development, tailoring to specific geographies and experimental investigation of management interventions.

Counting Cats: The integration of expert and citizen science data for unbiased inference of population abundance.

Free-roaming animal populations are hard to count, and professional experts are a limited resource. There is vast untapped potential in the data collected by nonprofessional scientists who volunteer their time to population monitoring, but citizen science (CS) raises concerns around data quality and biases. A particular concern in abundance modeling is the presence of false positives that can occur due to misidentification of nontarget species. Here, we introduce Integrated Abundance Models (IAMs) that integrate citizen and expert data to allow robust inference of population abundance meanwhile accounting for biases caused by misidentification. We used simulation experiments to confirm that IAMs successfully remove the inflation of abundance estimates caused by false-positive detections and can provide accurate estimates of both bias and abundance. We illustrate the approach with a case study on unowned domestic cats, which are commonly confused with owned, and infer their abundance by analyzing a combination of CS data and expert data. Our case study finds that relying on CS data alone, either through simple summation or via traditional modeling approaches, can vastly inflate abundance estimates. IAMs provide an adaptable framework, increasing the opportunity for further development of the approach, tailoring to specific systems and robust use of CS data.

Temporal consistency in herbivore responses to glucosinolate polymorphism in populations of wild cabbage (Brassica oleracea).

Natural populations of wild cabbage (Brassica oleracea) show significant qualitative diversity in heritable aliphatic glucosinolates, a class of secondary metabolites involved in defence against herbivore attack. One candidate mechanism for the maintenance of this diversity is that differential responses among herbivore species result in a net fitness balance across plant chemotypes. Such top-down differential selection would be promoted by consistent responses of herbivores to glucosinolates, temporal variation in herbivore abundance, and fitness impacts of herbivore attack on plants varying in glucosinolate profile. A 1-year survey across 12 wild cabbage populations demonstrated differential responses of herbivores to glucosinolates. We extended this survey to investigate the temporal consistency of these responses, and the extent of variation in abundance of key herbivores. Within plant populations, the aphid Brevicoryne brassicae consistently preferred plants producing the glucosinolate progoitrin. Among populations, increasing frequencies of sinigrin production correlated positively with herbivory by whitefly Aleyrodes proletella and negatively with herbivory by snails. Two Pieris butterfly species showed no consistent response to glucosinolates among years. Rates of herbivory varied significantly among years within populations, but the frequency of herbivory at the population scale varied only for B. brassicae. B. brassicae emerges as a strong candidate herbivore to impose differential selection on glucosinolates, as it satisfies the key assumptions of consistent preferences and heterogeneity in abundance. We show that variation in plant secondary metabolites structures the local herbivore community and that, for some key species, this structuring is consistent over time. We discuss the implications of these patterns for the maintenance of diversity in plant defence chemistry.

Migrant birds and mammals live faster than residents.

Billions of vertebrates migrate to and from their breeding grounds annually, exhibiting astonishing feats of endurance. Many such movements are energetically costly yet there is little consensus on whether or how such costs might influence schedules of survival and reproduction in migratory animals. Here we provide a global analysis of associations between migratory behaviour and vertebrate life histories. After controlling for latitudinal and evolutionary patterns, we find that migratory birds and mammals have faster paces of life than their non-migratory relatives. Among swimming and walking species, migrants tend to have larger body size, while among flying species, migrants are smaller. We discuss whether pace of life is a determinant, consequence, or adaptive outcome, of migration. Our findings have important implications for the understanding of the migratory phenomenon and will help predict the responses of bird and mammal species to environmental change.

Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities.

Natural plant populations often show substantial heritable variation in chemical structure of secondary metabolites. Despite a great deal of evidence from laboratory studies that these chemicals influence herbivore behaviour and life history, there exists little evidence for the structuring of natural herbivore communities according to plant chemical profiles. Brassica oleracea (Brassicaceae) produces aliphatic glucosinolates, which break down into toxins when leaf tissue is damaged. Structural diversity in these glucosinolates is heritable, and varies considerably at two ecological scales in the UK: both within and between populations. We surveyed herbivore attack on plants producing different glucosinolates, using 12 natural B. oleracea populations. In contrast to the results of previous studies in this system, which suffered low statistical power, we found significant differential responses of herbivore species to heritable glucosinolates, both within and between plant populations. We found significant correlations between herbivore infestation rates and the presence or absence of two heritable glucosinolates: sinigrin and progoitrin. There was variation between herbivore species in the direction of response, the ecological scale at which responses were identified, and the correlations for some herbivore species changed at different times of the year. We conclude that variation in plant secondary metabolites can structure the community of herbivores that attack them, and propose that herbivore-mediated differential selection deserves further investigation as a mechanism maintaining the observed diversity of glucosinolates in wild Brassica.

The organophosphorous pesticide, fenitrothion, acts as an anti-androgen and alters reproductive behavior of the male three-spined stickleback, Gasterosteus aculeatus.

Fenitrothion (FN) is a widely used organophosphorous pesticide that has structural similarities with the clinical anti-androgen flutamide. The potential for FN to act as an anti-androgen (at exposures of 1, 50, and 200 microg FN/l over a 26-day period) was assessed in male three-spined sticklebacks, Gasterosteus aculeatus, by measuring kidney spiggin concentration, nest-building, and courtship behavior. Spiggin is the glue protein that male sticklebacks use to build their nests and is directly controlled by androgens. FN exposure significantly reduced spiggin production as well as nest-building activity. It also adversely affected courtship--especially the 'zigzag dance' and biting behavior of the males. FN thus appears to have anti-androgenic effects on both the physiology and behavior of the male stickleback.