Population structure and genetic variation in the endangered Giant Kangaroo Rat (<Emphasis Type="Italic">Dipodomys ingens</Emphasis>)

Populations of the endangered giant kangaroo rat, Dipodomys ingens (Heteromyidae), have suffered increasing fragmentation and isolation over the recent past, and the distribution of this unique rodent has become restricted to 3% of its historical range. Such changes in population structure can significantly affect effective population size and dispersal, and ultimately increase the risk of extinction for endangered species. To assess the fine-scale population structure, gene flow, and genetic diversity of remnant populations of Dipodomys ingens, we examined variation at six microsatellite DNA loci in 95 animals from six populations. Genetic subdivision was significant for both the northern and southern part of the kangaroo rat’s range although there was considerable gene flow among southern populations. While regional gene diversity was relatively high for this endangered species, hierarchical F-statistics of northern populations in Fresno and San Benito counties suggested non-random mating and genetic drift within subpopulations. We conclude that effective dispersal, and therefore genetic distances between populations, is better predicted by ecological conditions and topography of the environment than linear geographic distance between populations. Our results are consistent with and complimentary to previous findings based on mtDNA variation of giant kangaroo rats. We suggest that management plans for this endangered rodent focus on protection of suitable habitat, maintenance of connectivity, and enhancement of effective dispersal between populations either through suitable dispersal corridors or translocations.     

Evaluation of assisted colonization strategies under global change for a rare,fire‐dependent plant

As a clear consensus is emerging that habitat for many species will dramatically reduce or shift with climate change, attention is turning to adaptation strategies to address these impacts. Assisted colonization is one such strategy that has been predominantly discussed in terms of the costs of introducing potential competitors into new communities and the benefits of reducing extinction risk. However, the success or failure of assisted colonization will depend on a range of population‐level factors that have not yet been quantitatively evaluated – the quality of the recipient habitat, the number and life stages of translocated individuals, the establishment of translocated individuals in their new habitat and whether the recipient habitat is subject to ongoing threats all will play an important role in population persistence. In this article, we do not take one side or the other in the debate over whether assisted colonization is worthwhile. Rather, we focus on the likelihood that assisted colonization will promote population persistence in the face of climate‐induced distribution changes and altered fire regimes for a rare endemic species. We link a population model with species distribution models to investigate expected changes in populations with climate change, the impact of altered fire regimes on population persistence and how much assisted colonization is necessary to minimize risk of decline in populations of Tecate cypress, a rare endemic tree in the California Floristic Province, a biodiversity hotspot. We show that assisted colonization may be a risk‐minimizing adaptation strategy when there are large source populations that are declining dramatically due to habitat contractions, multiple nearby sites predicted to contain suitable habitat, minimal natural dispersal, high rates of establishment of translocated populations and the absence of nonclimatic threats such as altered disturbance regimes. However, when serious ongoing threats exist, assisted colonization is ineffective.     

Proximity of restored hedgerows interacts with local floral diversity and species' traits to shape long‐term pollinator metacommunity dynamics

Disconnected habitat fragments are poor at supporting population and community persistence; restoration ecologists, therefore, advocate for the establishment of habitat networks across landscapes. Few empirical studies, however, have considered how networks of restored habitat patches affect metacommunity dynamics. Here, using a 10‐year study on restored hedgerows and unrestored field margins within an intensive agricultural landscape, we integrate occupancy modelling with network theory to examine the interaction between local and landscape characteristics, habitat selection and dispersal in shaping pollinator metacommunity dynamics. We show that surrounding hedgerows and remnant habitat patches interact with the local floral diversity, bee diet breadth and bee body size to influence site occupancy, via colonisation and persistence dynamics. Florally diverse sites and generalist, small‐bodied species are most important for maintaining metacommunity connectivity. By providing the first in‐depth assessment of how a network of restored habitat influences long‐term population dynamics, we confirm the conservation benefit of hedgerows for pollinator populations and demonstrate the importance of restoring and maintaining habitat networks within an inhospitable matrix.     

Conservation implications of a long-term decline in body condition of the Brothers Island tuatara (Sphenodon guntheri)

Understanding the factors that drive the dynamics of remnant populations of long-lived species presents a unique challenge for conservation management. The long-lived Brothers Island tuatara Sphenodon guntheri is represented by one natural, self-sustaining population on 4-ha North Brother Island, New Zealand, and two small, translocated populations. The North Brother Island population was almost driven to extinction by extreme habitat modification and collecting in the late 19th century. Analysis of a long-term (1957–2001) dataset, following the population's recovery, reveals a significant decline in tuatara body condition over time, which is more pronounced in females. Declining body condition, coupled with very low reproductive output, may be symptomatic of a density-dependent response to elevated population size exacerbated by resource limitation. Sex-specific effects that disadvantage females could compromise this small population, particularly as it exhibits a male-biased sex ratio. We recommend removal of infrequently used structures and habitat restoration to alleviate intense resource competition. Population-level manipulation should be considered if future monitoring indicates an increasingly male-biased sex ratio and continued decline of female body condition.     

Differential effects of spatial network structure and scale on population size and genetic diversity of the ninespine stickleback in a remnant wetland system

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Temporal genetic dynamics of reintroduced and translocated populations of the endangered golden lion tamarin (<Emphasis Type="Italic">Leontopithecus rosalia</Emphasis>)

Reintroductions—captive-born animals introduced into the species’ original distribution area—and translocations—free-living animals transferred to another location within the historical distribution area—are important conservation strategies for endangered species. Genetic analyses of 239 individuals from unmanaged, translocated and reintroduced populations of Leontopithecus rosalia were performed using 14 microsatellites. These samples were collected during two periods: (a) 1996–1997 (historic), when individuals were translocated and reintroduced into forest fragments in the lowland Atlantic Forest, and (b) 2007–09 (recent). We hypothesized that effective population size and genetic diversity would increase over time and that these management strategies would affect the resulting population genetic structure. We found trends indicating that the effective population size at the translocation site increased while that at the reintroduction sites diminished over time. The inbreeding coefficient of the translocated population diminished over time (from 0.38 to 0.03) and was much lower than that of the native (0.29) and reintroduced (0.13) recent populations. We observed a greater genetic admixture among the reintroduced sites on the historic sampling, as well as a strong genetic structure at the translocation site. In the recent sampling, the population structuring became more site-related suggesting low or inconsistent gene flow between sampling sites. This research highlights how conservation management decisions have an important influence on the genetic outcome of translocations and reintroductions. Future conservation planning should consider population genetic monitoring before and after management measures and maintain population connectivity thereafter to avoid the negative effects of a population size reduction.     

Predator dispersal determines the effect of connectivity on prey diversity

Linking local communities to a metacommunity can positively affect diversity by enabling immigration of dispersal-limited species and maintenance of sink populations. However, connectivity can also negatively affect diversity by allowing the spread of strong competitors or predators. In a microcosm experiment with five ciliate species as prey and a copepod as an efficient generalist predator, we analysed the effect of connectivity on prey species richness in metacommunities that were either unconnected, connected for the prey, or connected for both prey and predator. Presence and absence of predator dispersal was cross-classified with low and high connectivity. The effect of connectivity on local and regional richness strongly depended on whether corridors were open for the predator. Local richness was initially positively affected by connectivity through rescue of species from stochastic extinctions. With predator dispersal, however, this positive effect soon turned negative as the predator spread over the metacommunity. Regional richness was unaffected by connectivity when local communities were connected only for the prey, while predator dispersal resulted in a pronounced decrease of regional richness. The level of connectivity influenced the speed of richness decline, with regional species extinctions being delayed for one week in weakly connected metacommunities. While connectivity enabled rescue of prey species from stochastic extinctions, deterministic extinctions due to predation were not overcome through reimmigration from predator-free refuges. Prey reimmigrating into these sink habitats appeared to be directly converted into increased predator abundance. Connectivity thus had a positive effect on the predator, even when the predator was not dispersing itself. Our study illustrates that dispersal of a species with strong negative effects on other community members shapes the dispersal-diversity relationship. When connections enable the spread of a generalist predator, positive effects of connectivity on prey species richness are outweighed by regional extinctions through predation.     

Connectivity of prairie dog colonies in an altered landscape: inferences from analysis of microsatellite DNA variation

Connectivity of populations influences the degree to which species maintain genetic diversity and persist despite local extinctions. Natural landscape features are known to influence connectivity, but global anthropogenic landscape change underscores the importance of quantifying how human-modified landscapes disrupt connectivity of natural populations. Grasslands of western North America have experienced extensive habitat alteration, fragmenting populations of species such as black-tailed prairie dogs (Cynomys ludovicianus). Population sizes and the geographic range of prairie dogs have been declining for over a century due to habitat loss, disease, and eradication efforts. In many places, prairie dogs have persisted in the face of emerging urban landscapes that carve habitat into smaller and smaller fragments separated by uninhabitable areas. In extreme cases, prairie dog colonies are completely bounded by urbanization. Connectivity is particularly important for prairie dogs because colonies suffer high probabilities of extirpation by plague, and dispersal permits recolonization. Here we explore connectivity of prairie dog populations using analyses of 11 microsatellite loci for 9 prairie dog colonies spanning the fragmented landscape of Boulder County, Colorado. Isolation-by-resistance modeling suggests that wetlands and high intensity urbanization limit movement of prairie dogs. However, prairie dogs appear to move moderately well through low intensity development (including roads) and freely through cropland and grassland. Additionally, there is a marked decline in gene flow between colonies with increasing geographic distance, indicating isolation by distance even in an altered landscape. Our results suggest that prairie dog colonies retain some connectivity despite fragmentation by urbanization and agricultural development.     

Experimental translocation of juvenile water voles in a Scottish lowland metapopulation

Population density affects dispersal success because residents can hinder or facilitate immigration into a new site, via a “social fence effect” or “social attraction” (or “conspecific attraction”), respectively. These mechanisms can affect the dynamics of fragmented populations and the success of translocations. However, information on the settlement behaviour of dispersers is rare. We conducted a manipulative field experiment using wild water voles, which exist in metapopulations along waterways in Scotland. We translocated 17 young of dispersal age into either an occupied site or a vacant site containing good habitat, which had recently become extinct due to a feral predator (American mink) moving through. We monitored the movements of translocated voles using radio telemetry. Translocated voles were less likely to settle in occupied sites with higher densities of residents, suggesting a possible social fence effect at high density. There was evidence of a social attraction mechanism, because voles never remained at new sites unless another individual arrived soon after translocation, and they were more likely to settle in occupied or colonised sites than vacant ones. Voles remained in the transient phase of dispersal for many days, and often followed a “stepping stone” trajectory, stopping for several days at successive sites. We suggest that trajectories followed by dispersing water voles, the time scale and long dispersal distances found in this species are conducive to locating conspecifics at low density and colonising vacant habitat. These results are encouraging for prospects of metapopulation persistence and future translocation success.     

Determinants of extinction in fragmented plant populations: Crepis sancta (asteraceae) in urban environments

Local populations are subject to recurrent extinctions, and small populations are particularly prone to extinction. Both demographic (stochasticity and the Allee effect) and genetic factors (drift load and inbreeding depression) potentially affect extinction. In fragmented populations, regular dispersal may boost population sizes (demographic rescue effect) or/and reduce the local inbreeding level and genetic drift (genetic rescue effect), which can affect extinction risks. We studied extinction processes in highly fragmented populations of the common species Crepis sancta (Asteraceae) in urban habitats exhibiting a rapid turnover of patches. A four-year demographic monitoring survey and microsatellite genotyping of individuals allowed us to study the determinants of extinction. We documented a low genetic structure and an absence of inbreeding (estimated by multilocus heterozygosity), which suggest that genetic factors were not a major cause of patch extinction. On the contrary, local population size was the main factor in extinction, whereas connectivity was shown to decrease patch extinction, which we interpreted as a demographic rescue effect that was likely due to better pollination services for reproduction. This coupling of demographic and genetic tools highlighted the importance of dispersal in local patch extinctions of small fragmented populations connected by gene flow.     

Population genetic connectivity of an endemic New Zealand passerine after large‐scale local extirpations: a model of re‐colonization potential

Little is known about how a 70% loss of native forests has affected the genetic connectivity of remnant bird populations in New Zealand. We use the common and widely distributed New Zealand Bellbird Anthornis melanura as an indicator species of population connectivity for well‐flighted birds. Using eight microsatellite loci, we identified five main genetic populations in the North Island, South Island, sub‐Antarctic Auckland Islands and two small remnant island populations adjacent to a large region of avian extirpations in northern North Island. Only one remnant island population, on a 30‐year‐old conservation reserve at Tiritiri Matangi, displayed a clear signature of recent genetic bottleneck. The 7% migration rate at Tiritiri Matangi indicates that bottlenecks can be maintained despite habitat rehabilitation, possibly through behavioural barriers to gene flow. Adjacent to the same extirpation zone, Bellbirds on the Poor Knights Islands were found to have low genetic diversity and low re‐colonization potential. Two gaps concordant with deforestation patterns separated the Kapiti Coast of southern North Island from populations to both the north and the south. In summary, we identified linked avian habitats, as well as isolated and inbred populations and suggest that Bellbirds are good re‐colonizers. We emphasize the importance of genetic studies that assess animal dispersal among newly rehabilitated habitat patches.     

Translocations maintain genetic diversity and increase connectivity in sea otters,Enhydra lutris

Sea otters, Enhydra lutris, were once abundant along the nearshore areas of the North Pacific. The international maritime fur trade that ended in 1911 left 13 small remnant populations with low genetic diversity. Subsequent translocations into previously occupied habitat resulted in several reintroduced populations along the coast of North America. We sampled sea otters between 2008 and 2011 throughout much of their current range and used 19 nuclear microsatellite markers to evaluate genetic diversity, population structure, and connectivity between remnant and reintroduced populations. Average genetic diversity within populations was similar: observed heterozygosity 0.55 and 0.53, expected heterozygosity 0.56 and 0.52, unbiased expected heterozygosity 0.57 and 0.52, for reintroduced and remnant populations, respectively. Sea otter population structure was greatest between the Northern and Southern sea otters with further structuring in Northern sea otters into Western, Central, and Southeast populations (including the reintroduced populations). Migrant analyses suggest the successful reintroductions and growth of remnant groups have enhanced connectivity and gene flow between populations throughout many of the sampled Northern populations. We recommend that future management actions for the Southern sea otter focus on future reintroductions to fill the gap between the California and Washington populations ultimately restoring gene flow to the isolated California population.     

Fresh start after rough rides: understanding patterns of genetic differentiation upon human-mediated translocations

Biological invasions via translocations are a textbook case of globalization’s impact on species distributions. Human-mediated transport helps species to overcome natural spatial boundaries and establish populations, often from a small number of individuals, in ecosystems previously unreachable through natural range expansion. The result is a discontinuous species distribution, with connectivity between the native and non-native range dependent on the recurrence of human-mediated species movement. The genetic diversity of introduced individuals represents a random fraction of the original diversity in the native range, but because connectivity is lost, non-native populations are bound to evolve independently. As a result, translocations can reshuffle genetic diversity in non-native populations, and thus, differentiation patterns arising after introduction may constitute the first step of novel evolutionary trajectories. By performing a meta-analysis on 5516 mitochondrial sequences of 20 different species, we explored whether life- and evolutionary history could explain differentiation among non-native populations of recently translocated organisms. We observed a general pattern consisting of reduced differentiation among non-native populations whose introduction derived from a single and intentional translocation, suggesting that these human actions play a role in reshaping genetic variance in non-native ranges. Additionally, we found geographic distance to be a poor predictor of population differentiation on the non-native range when compared to averaged evolutionary distances—the opposite being true for the native range—reinforcing connectivity break imposed by translocation events. Understanding the factors driving the distribution of genetic diversity upon translocations might not only facilitate the development of plans to mitigate the dispersal of invasive species but also to explore the emergence of novel evolutionary trajectories.

     

Low diversity and high levels of population genetic structuring in introduced eastern mosquitofish (<Emphasis Type="Italic">Gambusia holbrooki</Emphasis>) in the greater Melbourne area,Australia

Eastern mosquitofish (Gambusia holbrooki) were introduced into Australia in 1925 and released to control mosquitoes. Gambusia holbrooki rapidly became invasive in recipient environments and now threaten native fauna. In this study, we used five polymorphic microsatellite loci and sequence from two mitochondrial genes, cytochrome b and cytochrome oxidase I, to evaluate genetic variation, colonisation and movement patterns of introduced G. holbrooki in the greater Melbourne area, and to assist in identifying the feasibility of local eradication. Microsatellite variation was consistently low within populations and there was evidence of bottleneck events for several populations. Populations displayed significant structuring associated with river basins rather than geographic distance, suggesting that habitat connectivity is important for dispersal. However, a few populations within river basins were more closely related to populations in other river basins than within their own basin, most likely reflecting a role of human-assisted dispersal in population establishment. Mitochondrial sequencing revealed only a single haplotype and suggested all populations were founded by individuals from a common source. These genetic data help delineate boundaries for local management strategies.     

Does colonization asymmetry matter in metapopulations?

Despite the considerable evidence showing that dispersal between habitat patches is often asymmetric, most of the metapopulation models assume symmetric dispersal. In this paper, we develop a Monte Carlo simulation model to quantify the effect of asymmetric dispersal on metapopulation persistence. Our results suggest that metapopulation extinctions are more likely when dispersal is asymmetric. Metapopulation viability in systems with symmetric dispersal mirrors results from a mean field approximation, where the system persists if the expected per patch colonization probability exceeds the expected per patch local extinction rate. For asymmetric cases, the mean field approximation underestimates the number of patches necessary for maintaining population persistence. If we use a model assuming symmetric dispersal when dispersal is actually asymmetric, the estimation of metapopulation persistence is wrong in more than 50% of the cases. Metapopulation viability depends on patch connectivity in symmetric systems, whereas in the asymmetric case the number of patches is more important. These results have important implications for managing spatially structured populations, when asymmetric dispersal may occur. Future metapopulation models should account for asymmetric dispersal, while empirical work is needed to quantify the patterns and the consequences of asymmetric dispersal in natural metapopulations.     

Fine-scale genetic structure of a long-lived reptile reflects recent habitat modification

Anthropogenic habitat fragmentation — ubiquitous in modern ecosystems — has strong impacts on gene flow and genetic population structure. Reptiles may be particularly susceptible to the effects of fragmentation because of their extreme sensitivity to environmental conditions and limited dispersal. We investigate fine-scale spatial genetic structure, individual relatedness, and sex-biased dispersal in a large population of a long-lived reptile (tuatara, Sphenodon punctatus) on a recently fragmented island. We genotyped individuals from remnant forest, regenerating forest, and grassland pasture sites at seven microsatellite loci and found significant genetic structuring (R_ST = 0.012) across small distances (< 500 m). Isolation by distance was not evident, but rather, genetic distance was weakly correlated with habitat similarity. Only individuals in forest fragments were correctly assignable to their site of origin, and individual pairwise relatedness in one fragment was significantly higher than expected. We did not detect sex-biased dispersal, but natural dispersal patterns may be confounded by fragmentation. Assignment tests showed that reforestation appears to have provided refuges for tuatara from disturbed areas. Our results suggest that fine-scale genetic structuring is driven by recent habitat modification and compounded by the sedentary lifestyle of these long-lived reptiles. Extreme longevity, large population size, simple social structure and random dispersal are not strong enough to counteract the genetic structure caused by a sedentary lifestyle. We suspect that fine-scale spatial genetic structuring could occur in any sedentary species with limited dispersal, making them more susceptible to the effects of fragmentation.     

Reconstructing the evolutionary history of an endangered subspecies across the changing landscape of the Great Central Valley of California

Identifying historic patterns of population genetic diversity and connectivity is a primary challenge in efforts to re‐establish the processes that have generated and maintained genetic variation across natural landscapes. The challenge of reconstructing pattern and process is even greater in highly altered landscapes where population extinctions and dramatic demographic fluctuations in remnant populations may have substantially altered, if not eliminated, historic patterns. Here, we seek to reconstruct historic patterns of diversity and connectivity in an endangered subspecies of woodrat that now occupies only 1–2 remnant locations within the highly altered landscape of the Great Central Valley of California. We examine patterns of diversity and connectivity using 14 microsatellite loci and sequence data from a mitochondrial locus and a nuclear intron. We reconstruct temporal change in habitat availability to establish several historical scenarios that could have led to contemporary patterns of diversity, and use an approximate Bayesian computation approach to test which of these scenarios is most consistent with our observed data. We find that the Central Valley populations harbour unique genetic variation coupled with a history of admixture between two well‐differentiated species of woodrats that are currently restricted to the woodlands flanking the Valley. Our simulations also show that certain commonly used analytical approaches may fail to recover a history of admixture when populations experience severe bottlenecks subsequent to hybridization. Overall our study shows the strength of combining empirical and simulation analyses to recover the history of populations occupying highly altered landscapes.     

Evaluating the role of environmental familiarity and behaviour in the success of wildlife translocation: A grizzly bear case study using agent-based modelling

Human-carnivore systems are built on multi-scalar complex processes often resulting in conflicts that force wildlife managers to address what are conceived as problem individuals. In North America, the grizzly bear (Ursus arctos) is often involved in human-bear conflict with management measures such as translocations, in which problem individuals are moved to new areas, being used to reduce conflict risk. While translocations offer a non-lethal alternative to managing conflict animals, they show varying levels of success. Our objective was to perform a novel assessment of grizzly bear translocation success through agent-based simulation by evaluating how familiarity with landscape features coupled with behavioral traits affects the way individuals use resources in a new environment. Our results showed that bears translocated to familiar habitat used high-quality habitat more than bears moved to areas with unfamiliar landscape characteristics. Increased exploration led to greater use of high-quality habitat in the long run but resulted in reduced use of high-quality habitat during the first two years following a translocation. Habitat quality use depended on scale, with bears translocated to less familiar environments accessing higher quality areas at a finer scale than bears translocated to familiar habitats. We emphasize the need to account for wildlife behavioral traits and habitat characteristics at multiple scales when selecting suitable translocation locations. Understanding the role of factors such as these on translocation outcome will help ensure the success of translocations not only as a method for managing problem wildlife, but also for population restoration, species reestablishment, and conservation translocations across the globe.     

No evidence for loss of genetic variation following sequential translocations in extant populations of a genetically depauperate species

Repeated population bottlenecks can lead to loss of genetic variation and normally should be avoided in threatened species to preserve evolutionary potential. We examined the effect of repeated bottlenecks, in the form of sequential translocations, on loss of genetic variation in a threatened passerine, the saddleback (Philesturnus carunculatus carunculatus), a species that has recovered from a remnant population with historically low levels of genetic variation. Although a slight but nonsignificant loss of alleles may have occurred between the first-order translocation and the extirpated source population, first-, second-, and third-order translocated populations had very similar levels of genetic variation to each other. The most obvious difference among the seven island populations appeared to lie in allele frequencies with little or no loss of alleles among extant populations. Although sequential translocations are known to cause loss of variation in genetically diverse species, our study indicates that genetically depauperate species may be less sensitive to loss of genetic variation through founder events presumably because the few remaining alleles are well represented in founding individuals. These results show that ancient bottlenecks may have a long-term effect on genetic variation, to the extent that contemporary population bottlenecks may leave no appreciable genetic signature. Our results suggest that subjecting genetically depauperate endangered species to sequential translocations could be used to rapidly establish new populations without further eroding genetic variation.     

The evolution of dispersal – the importance of information about population density and habitat characteristics

The evolution of mobility patterns and dispersal strategies depend on different population, habitat and life history characteristics. The ability to perceive and make use of information about the surrounding environment for dispersal decisions will also differ between organisms. To investigate the evolutionary consequences of such differences, we have used a simulation model with nearest-neighbour dispersal in a metapopulation to study how variation in the ability to obtain and make use of information about habitat quality and conspecific density affects the evolution of dispersal strategies. We found a rather strong influence of variation in information on the overall rate of dispersal in a metapopulation. The highest emigration rate evolved in organisms with no information about either density or habitat quality and the lowest rate was found in organisms with information about both the natal and the neighbouring patches. For organisms that can make use of information about conspecific density, positively density-dependent dispersal evolved in the majority of cases, with the strongest density dependence occurring when an individual only has information about density in the natal patch. However, we also identified situations, involving strong local population fluctuations and frequent local extinctions, where negatively density-dependent dispersal evolved.