Predicting the Probability of Outbreeding Depression

Abstract: Fragmentation of animal and plant populations typically leads to genetic erosion and increased probability of extirpation. Although these effects can usually be reversed by re‐establishing gene flow between population fragments, managers sometimes fail to do so due to fears of outbreeding depression (OD). Rapid development of OD is due primarily to adaptive differentiation from selection or fixation of chromosomal variants. Fixed chromosomal variants can be detected empirically. We used an extended form of the breeders’ equation to predict the probability of OD due to adaptive differentiation between recently isolated population fragments as a function of intensity of selection, genetic diversity, effective population sizes, and generations of isolation. Empirical data indicated that populations in similar environments had not developed OD even after thousands of generations of isolation. To predict the probability of OD, we developed a decision tree that was based on the four variables from the breeders’ equation, taxonomic status, and gene flow within the last 500 years. The predicted probability of OD in crosses between two populations is elevated when the populations have at least one of the following characteristics: are distinct species, have fixed chromosomal differences, exchanged no genes in the last 500 years, or inhabit different environments. Conversely, the predicted probability of OD in crosses between two populations of the same species is low for populations with the same karyotype, isolated for <500 years, and that occupy similar environments. In the former case, we recommend crossing be avoided or tried on a limited, experimental basis. In the latter case, crossing can be carried out with low probability of OD. We used crosses with known results to test the decision tree and found that it correctly identified cases where OD occurred. Current concerns about OD in recently fragmented populations are almost certainly excessive.     

Roads,Interrupted Dispersal,and Genetic Diversity in Timber Rattlesnakes

Abstract: Anthropogenic habitat modification often creates barriers to animal movement, transforming formerly contiguous habitat into a patchwork of habitat islands with low connectivity. Roadways are a feature of most landscapes that can act as barriers or filters to migration among local populations. Even small and recently constructed roads can have a significant impact on population genetic structure of some species, but not others. We developed a research approach that combines fine‐scale molecular genetics with behavioral and ecological data to understand the impacts of roads on population structure and connectivity. We used microsatellite markers to characterize genetic variation within and among populations of timber rattlesnakes (Crotalus horridus) occupying communal hibernacula (dens) in regions bisected by roadways. We examined the impact of roads on seasonal migration, genetic diversity, and gene flow among populations. Snakes in hibernacula isolated by roads had significantly lower genetic diversity and higher genetic differentiation than snakes in hibernacula in contiguous habitat. Genetic‐assignment analyses revealed that interruption to seasonal migration was the mechanism underlying these patterns. Our results underscore the sizeable impact of roads on this species, despite their relatively recent construction at our study sites (7 to 10 generations of rattlesnakes), the utility of population genetics for studies of road ecology, and the need for mitigating effects of roads.     

Human Influence and Classical Biogeographic Predictors of Rare Species Occurrence

Biogeographic theory predicts that rare species occur more often in larger, less‐isolated habitat patches and suggests that patch size and connectivity are positive predictors of patch quality for conservation. However, in areas substantially modified by humans, rare species may be relegated to the most isolated patches. We used data from plant surveys of 81 meadow patches in the Georgia Basin of Canada and the United States to show that presence of threatened and endangered plants was positively predicted for patches that were isolated on small islands surrounded by ocean and for patches that were isolated by surrounding forest. Neither patch size nor connectivity were positive predictors of rare species occurrence. Thus, in our study area, human influence, presumably due to disturbance or introduction of competitive non‐native species, appears to have overwhelmed classical predictors of rare species distribution, such that greater patch isolation appeared to favor presence of rare species. We suggest conservation planners consider the potential advantages of protecting geographically isolated patches in human‐modified landscapes because such patches may represent the only habitats in which rare species are likely to persist. Influencia Humana y Predictores Biogeográficos Clásicos de la Ocurrencia de Especies Raras     

Temporal Analysis of Genetic Structure to Assess Population Dynamics of Reintroduced Swift Foxes

Reintroductions are increasingly used to reestablish species, but a paucity of long‐term postrelease monitoring has limited understanding of whether and when viable populations subsequently persist. We conducted temporal genetic analyses of reintroduced populations of swift foxes (Vulpes velox) in Canada (Alberta and Saskatchewan) and the United States (Montana). We used samples collected 4 years apart, 17 years from the initiation of the reintroduction, and 3 years after the conclusion of releases. To assess program success, we genotyped 304 hair samples, subsampled from the known range in 2000 and 2001, and 2005 and 2006, at 7 microsatellite loci. We compared diversity, effective population size, and genetic connectivity over time in each population. Diversity remained stable over time and there was evidence of increasing effective population size. We determined population structure in both periods after correcting for differences in sample sizes. The geographic distribution of these populations roughly corresponded with the original release locations, which suggests the release sites had residual effects on the population structure. However, given that both reintroduction sites had similar source populations, habitat fragmentation, due to cropland, may be associated with the population structure we found. Although our results indicate growing, stable populations, future connectivity analyses are warranted to ensure both populations are not subject to negative small‐population effects. Our results demonstrate the importance of multiple sampling years to fully capture population dynamics of reintroduced populations. Análisis Temporal de la Estructura Genética para Evaluar la Dinámica Poblacional de Zorros (Vulpes velox) Reintroducidos     

Evidence of Local Adaptation in the Demographic Response of American Ginseng to Interannual Temperature Variation

Abstract: Bioclimatic envelope models of species’ responses to climate change are used to predict how species will respond to increasing temperatures. These models are frequently based on the assumption that the northern and southern boundaries of a species’ range define its thermal niche. However, this assumption may be violated if populations are adapted to local temperature regimes and have evolved population‐specific thermal optima. Considering the prevalence of local adaptation, the assumption of a species‐wide thermal optimum may be violated for many species. We used spatially and temporally extensive demographic data for American ginseng (Panax quinquefolius L.) to examine range‐wide variation in response of population growth rate (λ) to climatic factors. Our results suggest adaptation to local temperature, but not precipitation. For each population, λ was maximized when annual temperatures were similar to site‐specific, long‐term mean temperatures. Populations from disparate climatic zones responded differently to temperature variation, and there was a linear relation between population‐level thermal optima and the 30‐year mean temperature at each site. For species that are locally adapted to temperature, bioclimatic envelope models may underestimate the extent to which increasing temperatures will decrease population growth rate. Because any directional change from long‐term mean temperatures will decrease population growth rates, all populations throughout a species’ range will be adversely affected by temperature increase, not just populations at southern and low‐elevation boundaries. Additionally, when a species’ local thermal niche is narrower than its range‐wide thermal niche, a smaller temperature increase than would be predicted by bioclimatic envelope approaches may be sufficient to decrease population growth.     

Aligning science and policy to achieve evolutionarily enlightened conservation

There is increasing recognition among conservation scientists that long‐term conservation outcomes could be improved through better integration of evolutionary theory into management practices. Despite concerns that the importance of key concepts emerging from evolutionary theory (i.e., evolutionary principles and processes) are not being recognized by managers, there has been little effort to determine the level of integration of evolutionary theory into conservation policy and practice. We assessed conservation policy at 3 scales (international, national, and provincial) on 3 continents to quantify the degree to which key evolutionary concepts, such as genetic diversity and gene flow, are being incorporated into conservation practice. We also evaluated the availability of clear guidance within the applied evolutionary biology literature as to how managers can change their management practices to achieve better conservation outcomes. Despite widespread recognition of the importance of maintaining genetic diversity, conservation policies provide little guidance about how this can be achieved in practice and other relevant evolutionary concepts, such as inbreeding depression, are mentioned rarely. In some cases the poor integration of evolutionary concepts into management reflects a lack of decision‐support tools in the literature. Where these tools are available, such as risk‐assessment frameworks, they are not being adopted by conservation policy makers, suggesting that the availability of a strong evidence base is not the only barrier to evolutionarily enlightened management. We believe there is a clear need for more engagement by evolutionary biologists with policy makers to develop practical guidelines that will help managers make changes to conservation practice. There is also an urgent need for more research to better understand the barriers to and opportunities for incorporating evolutionary theory into conservation practice.     

Effects of Habitat Fragmentation on Effective Dispersal of Florida Scrub‐Jays

Abstract: Studies comparing dispersal in fragmented versus unfragmented landscapes show that habitat fragmentation alters the dispersal behavior of many species. We used two complementary approaches to explore Florida Scrub‐Jay (Aphelocoma c?rulescens) dispersal in relation to landscape fragmentation. First, we compared dispersal distances of color‐marked individuals in intensively monitored continuous and fragmented landscapes. Second, we estimated effective dispersal relative to the degree of fragmentation (as inferred from two landscape indexes: proportion of study site covered with Florida Scrub‐Jay habitat and mean distance to nearest habitat patch within each study site) by comparing genetic isolation‐by‐distance regressions among 13 study sites having a range of landscape structures. Among color‐banded individuals, dispersal distances were greater in fragmented versus continuous landscapes, a result consistent with other studies. Nevertheless, genetic analyses revealed that effective dispersal decreases as the proportion of habitat in the landscape decreases. These results suggest that although individual Florida Scrub‐Jays may disperse farther as fragmentation increases, those that do so are less successful as breeders than those that disperse short distances. Our study highlights the importance of combining observational data with genetic inferences when evaluating the complex biological and life‐history implications of dispersal.     

Founder Effects,Inbreeding, and Loss of Genetic Diversity in Four Avian Reintroduction Programs

Abstract: The number of individuals translocated and released as part of a reintroduction is often small, as is the final established population, because the reintroduction site is typically small. Small founder and small resulting populations can result in population bottlenecks, which are associated with increased rates of inbreeding and loss of genetic diversity, both of which can affect the long‐term viability of reintroduced populations. I used information derived from pedigrees of four monogamous bird species reintroduced onto two different islands (220 and 259 ha) in New Zealand to compare the pattern of inbreeding and loss of genetic diversity among the reintroduced populations. Although reintroduced populations founded with few individuals had higher levels of inbreeding, as predicted, other factors, including biased sex ratio and skewed breeding success, contributed to high levels of inbreeding and loss of genetic diversity. Of the 10–58 individuals released, 4–25 genetic founders contributed at least one living descendent and yielded approximately 3–11 founder–genome equivalents (number of genetic founders assuming an equal contribution of offspring and no random loss of alleles across generations) after seven breeding seasons. This range is much lower than the 20 founder–genome equivalents recommended for captive‐bred populations. Although the level of inbreeding in one reintroduced population initially reached three times that of a closely related species, the long‐term estimated rate of inbreeding of this one population was approximately one‐third that of the other species due to differences in carrying capacities of the respective reintroduction sites. The increasing number of reintroductions to suitable areas that are smaller than those I examined here suggests that it might be useful to develop long‐term strategies and guidelines for reintroduction programs, which would minimize inbreeding and maintain genetic diversity.     

Effects of Forest Fragmentation on Seed Dispersal and Seedling Establishment in Ornithochorous Trees

Abstract: Habitat fragmentation increases seed dispersal limitation across the landscape and may also affect subsequent demographic stages such as seedling establishment. Thus, the development of adequate plans for forest restoration requires an understanding of mechanisms by which fragmentation hampers seed delivery to deforested areas and knowledge of how fragmentation affects the relationship between seed‐deposition patterns and seedling establishment. We evaluated the dispersal and recruitment of two bird‐dispersed, fleshy‐fruited tree species (Crataegus monogyna and Ilex aquifolium) in fragmented secondary forests of northern Spain. Forest fragmentation reduced the probability of seed deposition for both trees because of decreased availability of woody perches and fruit‐rich neighborhoods for seed dispersers, rather than because of reductions in tree cover by itself. The effects of fragmentation went beyond effects on the dispersal stage in Crataegus because seedling establishment was proportional to the quantities of bird‐dispersed seeds arriving at microsites. In contrast, postdispersal mortality in Ilex was so high that it obscured the seed‐to‐seedling transition. These results suggest that the effects of fragmentation are not necessarily consistent across stages of recruitment across species. Habitat management seeking to overcome barriers to forest recovery must include the preservation, and even the planting, of fleshy‐fruited trees in the unforested matrix as a measure to encourage frugivorous birds to enter into open and degraded areas. An integrative management strategy should also explicitly consider seed‐survival expectancies at microhabitats to preserve plant‐population dynamics and community structure in fragmented landscapes.     

Simulating Retention of Rare Alleles in Small Populations to Assess Management Options for Species with Different Life Histories

Preserving allelic diversity is important because it provides the capacity for adaptation and thus enables long‐term population viability. Allele retention is difficult to predict in animals with overlapping generations, so we used a new computer model to simulate retention of rare alleles in small populations of 3 species with contrasting life‐history traits: North Island Brown Kiwi (Apteryx mantelli; monogamous, long‐lived), North Island Robins (Petroica longipes; monogamous, short‐lived), and red deer (Cervus elaphus; polygynous, moderate lifespan). We simulated closed populations under various demographic scenarios and assessed the amounts of artificial immigration needed to achieve a goal of retaining 90% of selectively neutral rare alleles (frequency in the source population = 0.05) after 10 generations. The number of immigrants per generation required to meet the genetic goal ranged from 11 to 30, and there were key similarities and differences among species. None of the species met the genetic goal without immigration, and red deer lost the most allelic diversity due to reproductive skew among polygynous males. However, red deer required only a moderate rate of immigration relative to the other species to meet the genetic goal because nonterritorial breeders had a high turnover. Conversely, North Island Brown Kiwi needed the most immigration because the long lifespan of locally produced territorial breeders prevented a large proportion of immigrants from recruiting. In all species, the amount of immigration needed generally decreased with an increase in carrying capacity, survival, or reproductive output and increased as individual variation in reproductive success increased, indicating the importance of accurately quantifying these parameters to predict the effects of management. Overall, retaining rare alleles in a small, isolated population requires substantial investment of management effort. Use of simulations to explore strategies optimized for the populations in question will help maximize the value of this effort. Simulación de la Retención de Alelos Raros en Poblaciones Pequeñas para Evaluar Opciones de Manejo para Especies con Historias de Vida Diferentes     

Evaluating Alternative Strategies for Minimizing Unintended Fitness Consequences of Cultured Individuals on Wild Populations

Artificial propagation strategies often incur selection in captivity that leads to traits that are maladaptive in the wild. For propagation programs focused on production rather than demographic contribution to wild populations, effects on wild populations can occur through unintentional escapement or the need to release individuals into natural environments for part of their life cycle. In this case, 2 alternative management strategies might reduce unintended fitness consequences on natural populations: (1) reduce selection in captivity as much as possible to reduce fitness load (keep them similar), or (2) breed a separate population to reduce captive‐wild interactions as much as possible (make them different). We quantitatively evaluate these 2 strategies with a coupled demographic–genetic model based on Pacific salmon hatcheries that incorporates a variety of relevant processes and dynamics: selection in the hatchery relative to the wild, assortative mating based on the trait under selection, and different life cycle arrangements in terms of hatchery release, density dependence, natural selection, and reproduction. Model results indicate that, if natural selection only occurs between reproduction and captive release, the similar strategy performs better. However, if natural selection occurs between captive release and reproduction, the different and similar strategies present viable alternatives to reducing unintended fitness consequences because of the greater opportunity to purge maladaptive individuals. In this case, the appropriate approach depends on the feasibility of each strategy and the demographic goal (e.g., increasing natural abundance, or ensuring that a high proportion of natural spawners are naturally produced). In addition, the fitness effects of hatchery release are much greater if hatchery release occurs before (vs. after) density‐dependent interactions. Given the logistical challenges to achieving both the similar and different strategies, evaluation of not just the preferred strategy but also the consequences of failing to achieve the desired target is critical. Evaluación de Estrategias Alternativas para Minimizar las Consecuencias No Inesperadas en la Adecuación de Individuos Criados en Cautiverio sobre Poblaciones Silvestres     

Securing the Demographic and Genetic Future of Tuatara through Assisted Colonization

Abstract: Climate change poses a particular threat to species with fragmented distributions and little or no capacity to migrate. Assisted colonization, moving species into regions where they have not previously occurred, aims to establish populations where they are expected to survive as climatic envelopes shift. However, adaptation to the source environment may affect whether species successfully establish in new regions. Assisted colonization has spurred debate among conservation biologists and ecologists over whether the potential benefits to the threatened species outweigh the potential disruption to recipient communities. In our opinion, the debate has been distracted by controversial examples, rather than cases where assisted colonization may be a viable strategy. We present a strategic plan for the assisted migration of tuatara (Sphenodon punctatus), an endemic New Zealand reptile. The plan includes use of extant populations as reference points for comparisons with assisted‐colonization populations with respect to demography, phenotypic plasticity, and phenology; optimization of genetic variation; research to fill knowledge gaps; consideration of host and recipient communities; and inclusion of stakeholders in the planning stage. When strategically planned and monitored, assisted colonization could meet conservation and research goals and ultimately result in the establishment of long‐term sustainable populations capable of persisting during rapid changes in climate.     

Use of Experimental Translocations of Allegheny Woodrat to Decipher Causal Agents of Decline

Translocations are an important tool for wildlife conservation, although progress in the field of reintroduction biology has been hindered by the ad hoc and opportunistic nature of many translocations. We used an experimental translocation to elucidate the role of raccoon roundworm (Baylisascaris procyonis) and inbreeding depression in the decline of the Allegheny woodrat (Neotoma magister), an endangered species. We translocated woodrats from genetically diverse populations in the core of the species range to 4 previously occupied sites (reintroductions) and 2 sites supporting genetically depauperate populations (reinforcements) in Indiana (U.S.A.). In 2 reintroduction sites and 1 reinforcement site, we distributed anthelmintic baits to passively deworm raccoons and reduce the risk of woodrat exposure to roundworms. The remaining sites served as controls. We used raccoon latrine surveys and fecal flotation to monitor temporal variability in roundworm prevalence and effect of treatment. We used live trapping and microsatellite genotyping to monitor the demographic and genetic response of translocated populations over the following 54 months. At the conclusion of the study, 4 of 6 translocations were successfully maintaining abundance through local recruitment. The distribution of anthelmintic baits reduced levels of roundworm contamination, but levels of contamination were also low in 2 of 3 control sites. Reintroductions failed at control sites, one of which was due to high roundworm exposure. The other failed control reintroduction was likely attributable to demographic stochasticity and limited reproductive potential following initial mortality within the first 4 months. In both control and treatment reinforcements, increases in both allelic richness and heterozygosity were accompanied by increases in abundance, which is suggestive of genetic rescue. Our results demonstrate that mitigation of roundworm exposure through the distribution of anthelmintic baits can facilitate woodrat recovery and that diversity within genetically depauperate populations can be restored through the introduction of a limited number of individuals. El Uso de Reubicaciones Experimentales de Neotoma magister para Descifrar Agentes Causales de Disminución     

Hunting Effects on Favourable Conservation Status of Highly Inbred Swedish Wolves

The wolf (Canis lupus) is classified as endangered in Sweden by the Swedish Species Information Centre, which is the official authority for threat classification. The present population, which was founded in the early 1980s, descends from 5 individuals. It is isolated and highly inbred, and on average individuals are more related than siblings. Hunts have been used by Swedish authorities during 2010 and 2011 to reduce the population size to its upper tolerable level of 210 wolves. European Union (EU) biodiversity legislation requires all member states to promote a concept called “favourable conservation status” (FCS) for a series of species including the wolf. Swedish national policy stipulates maintenance of viable populations with sufficient levels of genetic variation of all naturally occurring species. Hunting to reduce wolf numbers in Sweden is currently not in line with national and EU policy agreements and will make genetically based FCS criteria less achievable for this species. We suggest that to reach FCS for the wolf in Sweden the following criteria need to be met: (1) a well‐connected, large, subdivided wolf population over Scandinavia, Finland, and the Russian Karelia‐Kola region should be reestablished, (2) genetically effective size (N_e) of this population is in the minimum range of N_e = 500–1000, (3) Sweden harbors a part of this total population that substantially contributes to the total N_e and that is large enough to not be classified as threatened genetically or according to IUCN criteria, and (4) average inbreeding levels in the Swedish population are <0.1. Efectos de la Cacería sobre el Estatus de Conservación Favorable de Lobos Suecos con Endogamia Alta     

Interacting Effects of Phenotypic Plasticity and Evolution on Population Persistence in a Changing Climate

Abstract: Climate change affects individual organisms by altering development, physiology, behavior, and fitness, and populations by altering genetic and phenotypic composition, vital rates, and dynamics. We sought to clarify how selection, phenotypic plasticity, and demography are linked in the context of climate change. On the basis of theory and results of recent empirical studies of plants and animals, we believe the ecological and evolutionary issues relevant to population persistence as climate changes are the rate, type, magnitude, and spatial pattern of climate‐induced abiotic and biotic change; generation time and life history of the organism; extent and type of phenotypic plasticity; amount and distribution of adaptive genetic variation across space and time; dispersal potential; and size and connectivity of subpopulations. An understanding of limits to plasticity and evolutionary potential across traits, populations, and species and feedbacks between adaptive and demographic responses is lacking. Integrated knowledge of coupled ecological and evolutionary mechanisms will increase understanding of the resilience and probabilities of persistence of populations and species.     

Phenological mismatch and the effectiveness of assisted gene flow

The persistence of narrowly adapted species under climate change will depend on their ability to migrate apace with their historical climatic envelope or to adapt in place to maintain fitness. This second path to persistence can only occur if there is sufficient genetic variance for response to new selection regimes. Inadequate levels of genetic variation can be remedied through assisted gene flow (AGF), that is the intentional introduction of individuals genetically adapted to localities with historic climates similar to the current or future climate experienced by the resident population. However, the timing of reproduction is frequently adapted to local conditions. Phenological mismatch between residents and migrants can reduce resident × migrant mating frequencies, slowing the introgression of migrant alleles into the resident genetic background and impeding evolutionary rescue efforts. Focusing on plants, we devised a method to estimate the frequency of resident × migrant matings based on flowering schedules and applied it in an experiment that mimicked the first generation of an AGF program with Chamaecrista fasciculata, a prairie annual, under current and expected future temperature regimes. Phenological mismatch reduced the potential for resident × migrant matings by 40–90%, regardless of thermal treatment. The most successful migrant sires were the most resident like in their flowering time, further biasing the genetic admixture between resident and migrant populations. Other loci contributing to local adaptation—heat‐tolerance genes, for instance—may be in linkage disequilibrium with phenology when residents and migrants are combined into a single mating pool. Thus, introgression of potentially adaptive migrant alleles into the resident genetic background is slowed when selection acts against migrant phenology. Successful AGF programs may require sustained high immigration rates or preliminary breeding programs when phenologically matched migrant source populations are unavailable.     

Determining the drivers of population structure in a highly urbanized landscape to inform conservation planning

Understanding the environmental contributors to population structure is of paramount importance for conservation in urbanized environments. We used spatially explicit models to determine genetic population structure under current and future environmental conditions across a highly fragmented, human‐dominated environment in Southern California to assess the effects of natural ecological variation and urbanization. We focused on 7 common species with diverse habitat requirements, home‐range sizes, and dispersal abilities. We quantified the relative roles of potential barriers, including natural environmental characteristics and an anthropogenic barrier created by a major highway, in shaping genetic variation. The ability to predict genetic variation in our models differed among species: 11–81% of intraspecific genetic variation was explained by environmental variables. Although an anthropogenically induced barrier (a major highway) severely restricted gene flow and movement at broad scales for some species, genetic variation seemed to be primarily driven by natural environmental heterogeneity at a local level. Our results show how assessing environmentally associated variation for multiple species under current and future climate conditions can help identify priority regions for maximizing population persistence under environmental change in urbanized regions.