Loss of genetic diversity in an outbreeding species: small population effects in the African wild dog <Emphasis Type="Italic">(Lycaon pictus</Emphasis>)

Genetic studies on the endangered African wild dog (Lycaon pictus) have primarily focused on the few remaining large and viable populations. However, investigations on the many isolated small African wild dog populations might also be informative for species management because the majority of extant populations are small and may contain genetic variability that is important for population persistence and for species conservation. Small populations are at higher risk of extinction from stochastic and deterministic demographic processes than larger populations and this is often of more immediate conservation concern than loss of genetic diversity, particularly for species that exhibit out-breeding behaviour such as long distance dispersal which may maintain gene flow. However, the genetic advantages of out-breeding behaviour may be reduced if dispersal is compromised beyond reserve borders (edge effects), further weakening the integrity of small populations. Mitochondrial DNA and 11 microsatellite genetic markers were used to investigate population genetic structure in a small population of out-breeding African wild dogs in Zambia, which occupies an historical dispersal corridor for the species. Results indicated the Zambian population suffered from low allelic richness, and there was significant evidence of a recent population bottleneck. Concurrent ecological data suggests these results were due to habitat fragmentation and restricted dispersal which compromised natural out-breeding mechanisms. This study recommends conservation priorities and management units for the African wild dog that focus on conserving remaining levels of genetic diversity, which may also be applicable for a range of out-breeding species.     

The devil's in the details: genetic and phenotypic divergence between artificial and native populations of the endangered pupfish (Cyprinodon diabolis)

Propagation of threatened or endangered species in artificial habitats is a common strategy for reducing the probability of extinction by demographic or stochastic forces. Differential selection, founder effects and genetic drift can conspire to cause artificial populations to differ irreversibly from native populations for characters important for fitness, thereby compromising conservation efforts. Here we show that artificial propagation of the endangered Devil's Hole pupfish Cyprinodon diabolis resulted in rapid divergence for phenotypic and genetic characteristics despite attempts to replicate key characteristics of the species' native habitat when designing the artificial environments. Although differences in behavior and morphology between the native pool population and the two artificial pools may reflect phenotypic plasticity, the results underscore the need to monitor and control (to the extent possible) closely the evolutionary process when propagating native species in artificial pools for multiple generations.     

海洋岛屿生物多样性保育研究进展

海洋岛屿生态系统因具有明显的海域地理隔离而区别于陆地生态系统,被誉为生物地理与进化生态学研究的"天然实验室".陆地或其它邻近岛屿的种源物种迁移到新的岛屿后,经历地理隔离、特征置换或适应辐射等一系列的岛屿进化过程,形成与种源物种具有显著遗传差异的岛屿特有种.岛屿在小面积范围内分化形成大量的特有种,是岛屿生物多样性最为重要的特点之一.但是,岛屿种群由于分布范围局限、生境脆弱且种群规模较小,岛屿种群较陆地种群具有更高的灭绝风险.本文通过对海洋岛屿物种的起源与演化、遗传结构以及岛屿物种的濒危与保护3个热点问题的讨论,阐述岛屿生物多样性的形成机制、濒危肇因以及岛屿生物多样性保育的重要性.     

Conservation implications of hybridization in Hawaiian picture-winged Drosophila

In this review, we discuss the importance of hybridization among species for the conservation of Hawaiian picture-winged Drosophila. Hybridization can be a positive evolutionary process that creates new species and increases the adaptation of populations and species through the spread of adaptive alleles and traits. Conversely, hybridization can disrupt the genetic integrity of species or populations and this may be most detrimental among taxa that are recently hybridizing due to recent ecological changes. The loss of biodiversity in Hawaiian Drosophila through hybridization may be facilitated by habitat alteration and introduced species that reduce population sizes and alter geographic distributions of native species. We briefly review the evidence for hybridization in the genus Drosophila and then focus on hybridization in the Hawaiian picture-winged Drosophila. We examine three general approaches for identifying hybrids and for assessing the factors that appear to contribute to hybridization and the potential ecological and evolutionary outcomes of hybrids in natural populations. Overall, the potential for hybridization among species will likely increase the risk of extinction for Hawaiian picture-winged Drosophila species. Thus, it is important to consider the potential for hybridization among species when developing plans for the conservation of Hawaiian Drosophila.     

Habitat specialization predicts genetic response to fragmentation in tropical birds

Habitat fragmentation is one of the most severe threats to biodiversity as it may lead to changes in population genetic structure, with ultimate modifications of species evolutionary potential and local extinctions. Nonetheless, fragmentation does not equally affect all species and identifying which ecological traits are related to species sensitivity to habitat fragmentation could help prioritization of conservation efforts. Despite the theoretical link between species ecology and extinction proneness, comparative studies explicitly testing the hypothesis that particular ecological traits underlies species‐specific population structure are rare. Here, we used a comparative approach on eight bird species, co‐occurring across the same fragmented landscape. For each species, we quantified relative levels of forest specialization and genetic differentiation among populations. To test the link between forest specialization and susceptibility to forest fragmentation, we assessed species responses to fragmentation by comparing levels of genetic differentiation between continuous and fragmented forest landscapes. Our results revealed a significant and substantial population structure at a very small spatial scale for mobile organisms such as birds. More importantly, we found that specialist species are more affected by forest fragmentation than generalist ones. Finally, our results suggest that even a simple habitat specialization index can be a satisfying predictor of genetic and demographic consequences of habitat fragmentation, providing a reliable practical and quantitative tool for conservation biology.     

Evolution of population genetic structure of the British roe deer by natural and anthropogenic processes (Capreolus capreolus)

Human influence typically impacts on natural populations of conservation interest. These interactions are varied and sometimes complex, and may be negative and unintended or associated with conservation and management strategy. Understanding the details of how these interactions influence and are influenced by natural evolutionary processes is essential to the development of effective conservation strategies. In this study, we investigate a species in Britain that has experienced both negative impact through overhunting in historical times and management efforts through culls and translocations. At the same time, there are regional populations that have been less affected by human influence. We use mtDNA and nuclear microsatellite DNA markers to investigate patterns of connectivity and diversity and find multiple insular populations in Britain that probably evolved within the Holocene (when the habitat was free of ice). We identify three concurrent processes. First, surviving indigenous populations show highly provincial patterns of philopatry, maintaining and generating population structure on a small geographic scale. Second, founder populations into habitat extirpated of native populations have expanded, but remained largely insular. Third, introductions into established populations generate some admixture. We discuss the implications for the evolution of diversity of the integration of natural processes with anthropogenic influences on population size and distribution.     

Outbreeding depression and breeding system evolution in small,remnant populations of <Emphasis Type="Italic">Primula vulgaris</Emphasis>: consequences for genetic rescue

Many species suffer from anthropogenic habitat fragmentation. The resulting small and isolated populations are more prone to extinction due to, amongst others, genetic erosion, inbreeding depression and Allee-effects. Genetic rescue can help mitigate such problems, but might result in outbreeding depression. We evaluated offspring fitness after selfing and outcrossing within and among three very small and isolated remnant populations of the heterostylous plant Primula vulgaris. We used greenhouse-grown offspring from these populations to test several fitness components. One population was fixed for the pin-morph, and was outcrossed with another population in the field to obtain seeds. Genetic diversity of parent and offspring populations was studied using microsatellites. Morph and population-specific heterosis, inbreeding and outbreeding depression were observed for fruit and seed set, seed weight and cumulative fitness. Highest fitness was observed in the field-outcrossed F1-population, which also showed outbreeding depression following subsequent between-population (back)crossing. Despite outbreeding depression, fitness was still relatively high. Inbreeding coefficients indicated that the offspring were more inbred than their parent populations. Offspring heterozygosity and inbreeding coefficients correlated with observed fitness. One population is evolving homostyly, showing a thrum morph with an elongated style and high autonomous fruit and seed set. This has important implications for conservation strategies such as genetic rescue, as the mating system will be altered by the introduction of homostyles.     

Habitat fragmentation effects on fitness of plant populations – a review

Habitat fragmentation threatens the survival of many species and local populations. Habitat fragmentation has two major consequences: populations become more isolated and are reduced in size. Small compared with large populations have increased extinction risks because of different types stochasticity (e.g. genetic drift) and inbreeding, which can negatively affect the fitness of individuals or populations. Habitat fragmentation may also change the abiotic conditions of the surrounding landscape, which influences biotic interactions. This review gives an introduction to the theory of the effects of habitat fragmentation on mean fitness of plant populations. It intends to help bridge the gap between conservation biologists and conservation practitioners. The paper shortly introduces basic concepts of population biology, demography and genetics and cites relevant and new literature. Special attention is given to more common plant species, which have attracted far less conservation attention than rare species.     

Human-mediated processes affecting distribution and genetic structure of Squalidus multimaculatus,a freshwater cyprinid with small spatial range

Endemic species typically have a narrow niche breadth, and are likely more vulnerable to extinction than more widespread taxa. Squalidus multimaculatus is a small cyprinid endemic to the Korean Peninsula, and its reported geographical range was restricted to several small rivers located along the southeast coast. Several populations of S. multimaculatus have supposedly been subject to a variety of recent anthropogenic actions. Here, we analyzed the pattern of genetic diversity within and among populations of S. multimaculatus using nine microsatellite loci to quantify the relative contributions of human-mediated processes to the contemporary distribution and genetic structure. Overall, low levels of genetic diversity were exhibited in the populations of S. multimaculatus. Genetic differentiations among populations were not completely represented by their geographical proximity, likely resulting from the low intrapopulation genetic variability and anthropogenic transplants. The most conspicuous outcome of the anthropogenic activities was the introgression of alleles from a closely related species, S. gracilis majimae. Our study showed that anthropogenic transplanting, even with only a small number of individuals, can challenge our conservation goal to maintain the species integrity that has long been shaped in evolutionary processes.     

Hybridization in a warmer world

Climate change is profoundly affecting the evolutionary trajectory of individual species and ecological communities, in part through the creation of novel species assemblages. How climate change will influence competitive interactions has been an active area of research. Far less attention, however, has been given to altered reproductive interactions. Yet, reproductive interactions between formerly isolated species are inevitable as populations shift geographically and temporally as a result of climate change, potentially resulting in introgression, speciation, or even extinction. The susceptibility of hybridization rates to anthropogenic disturbance was first recognized in the 1930s. To date, work on anthropogenically mediated hybridization has focused primarily on either physical habitat disturbance or species invasion. Here, I review recent literature on hybridization to identify how ecological responses to climate change will increase the likelihood of hybridization via the dissolution of species barriers maintained by habitat, time, or behavior. Using this literature, I identify several cases where novel hybrid zones have recently formed, likely as a result of changing climate. Future research should focus on identifying areas and taxonomic groups where reproductive species interactions are most likely to be influenced by climate change. Furthermore, a better understanding of the evolutionary consequences of climate‐mediated secondary contact is urgently needed. Paradoxically, hybridization is both a major conservation concern and an important source of novel genetic and phenotypic variation. Hybridization may therefore both contribute to increasing rates of extinction and stimulate the creation of novel phenotypes that will speed adaptation to novel climates. Predicting which result will occur following secondary contact will be an important contribution to conservation for many species.     

Conservation genetics of the yellow-bellied toad (Bombina variegata): population structure,genetic diversity and landscape effects in an endangered amphibian

Revealing patterns of genetic diversity and barriers for gene flow are key points for successful conservation in endangered species. Methods based on molecular markers are also often used to delineate conservation units such as evolutionary significant units and management units. Here we combine phylo-geographic analyses (based on mtDNA) with population and landscape genetic analyses (based on microsatellites) for the endangered yellow-bellied toad Bombina variegata over a wide distribution range in Germany. Our analyses show that two genetic clusters are present in the study area, a northern and a southern/central one, but that these clusters are not deeply divergent. The genetic data suggest high fragmentation among toad occurrences and consequently low genetic diversity. Genetic diversity and genetic connectivity showed a negative relationship with road densities and urban areas surrounding toad occurrences, indicating that these landscape features act as barriers to gene flow. To preserve a maximum of genetic diversity, we recommend considering both genetic clusters as management units, and to increase gene flow among toad occurrences with the aim of restoring and protecting functional meta-populations within each of the clusters. Several isolated populations with especially low genetic diversity and signs of inbreeding need particular short-term conservation attention to avoid extinction. We also recommend to allow natural gene flow between both clusters but not to use individuals from one cluster for translocation or reintroduction into the other. Our results underscore the utility of molecular tools for species conservation, highlight outcomes of habitat fragmentation onto the genetic structure of an endangered amphibian and reveal particularly threatened populations in need for urgent conservation efforts.

     

Broken barriers: human-induced changes to gene flow and introgression in animals: an examination of the ways in which humans increase genetic exchange among populations and species and the consequences for biodiversity

We identify two processes by which humans increase genetic exchange among groups of individuals: by affecting the distribution of groups and dispersal patterns across a landscape, and by affecting interbreeding among sympatric or parapatric groups. Each of these processes might then have two different effects on biodiversity: changes in the number of taxa through merging or splitting of groups, and the extinction/extirpation of taxa through effects on fitness. We review the various ways in which humans are affecting genetic exchange, and highlight the difficulties in predicting the impacts on biodiversity. Gene flow and hybridization are crucially important evolutionary forces influencing biodiversity. Humans alter natural patterns of genetic exchange in myriad ways, and these anthropogenic effects are likely to influence the genetic integrity of populations and species. We argue that taking a gene-centric view towards conservation will help resolve issues pertaining to conservation and management. Editor's suggested further reading in BioEssays A systemic view of biodiversity and its conservation: Processes, interrelationships, and human culture Abstract.     

Naiveté and Novel Perturbations: Conservation of Native Spiders on an Oceanic Island System

The native fauna of isolated island systems is generally unique with acute conservation issues. For spiders in Hawaii, the first impediment to effective conservation is lack of taxonomic knowledge. The primary conservation concerns are related to the highly localized areas of endemicity of many species, with associated small population sizes. Species on insular systems tend to occur naturally in small populations, and small population size itself may not be a cause for conservation concern. However, for spiders and other arthropods, which tend to have shorter generation times compared to vertebrates, population fluctuations will tend to be more frequent, rendering them more vulnerable to extinction through demographic accidents at small population size. The knowledge we have to date suggests that habitat disturbance and alien species invasion are probably the major factors affecting native spiders in the islands. For a given natural community, the ability of species to accommodate habitat perturbation may be related more to the novelty of the perturbation than to its apparent severity. Although native spiders appear to tolerate disruption of the species composition of the native vegetation, evidence suggests that they are severely impacted by alien arthropod predators, in particular social hymenoptera, a group not represented among native Hawaiian arthropods.     

A metapopulation paradox: partial improvement of habitat may reduce metapopulation persistence

The adverse influence of habitat degradation on the survival of populations may sometimes be amplified by rapid evolution over ecological timescales. This phenomenon of "evolutionary suicide" has been described in theoretical as well as empirical studies. However, no studies have suggested that habitat improvement could possibly also trigger an evolutionary response that would result in a decline in population size. We use individual-based simulations to demonstrate the potential for such a paradoxical response. An increase in the quality, size, or stability of only a fraction of the habitat patches in a metapopulation may result in an evolutionary decline in the dispersal propensity of individuals, followed by a decrease in recolonization, a reduction in the number of patches occupied, a decline in overall population size, and even extinction. Thus, well-intended conservation efforts that ignore potential evolutionary consequences of habitat management may increase the extinction risk of populations.     

Effects of landscape and patch-level attributes on regional population persistence

Species responses are influenced by processes operating at multiple scales, yet many conservation studies and management actions are focused on a single scale. Although landscape-level habitat conditions (i.e., habitat amount, fragmentation and landscape quality) are likely to drive the regional persistence of spatially structured populations, patch-level factors (i.e., patch size, isolation, and quality) may also be important. To determine the spatial scales at which habitat factors influence the regional persistence of endangered Ord's kangaroo rats (Dipodomys ordii) in Alberta, Canada, we simulated population dynamics under a range of habitat conditions. Using a spatially-explicit population model, we removed groups of habitat patches based on their characteristics and measured the resulting time to extinction. We used proportional hazards models to rank the influence of landscape and interacting patch-level variables. Landscape quality was the most influential variable followed by patch quality, with both outweighing landscape- and patch-level measures of habitat quantity and fragmentation/proximity. Although habitat conservation and restoration priorities for this population should be in maximizing the overall quality of the landscape, population persistence depends on how this goal is achieved. Patch quality exerted a significant influence on regional persistence, with the removal of low quality road margin patches (sinks) reducing the risk of regional extinction. Strategies for maximizing overall landscape quality that omit patch-level considerations may produce suboptimal or detrimental results for regional population persistence, particularly where complex local population dynamics (e.g., source-sink dynamics) exist. This study contributes to a growing body literature that suggests that the prediction of species responses and future conservation actions may best be assessed with a multi-scale approach that considers habitat quality and that the success of conservation actions may depend on assessing the influences of habitat factors at multiple scales.     

An exceptional case of historical outbreeding in African sable antelope populations

Empirical investigations of intraspecific outbreeding and subsequent introgressive hybridization in natural populations are rare, particularly among conspecific populations of large mammals. Using mitochondrial DNA data [partial control region (496 basepairs - bp) and cytochrome b gene (343 bp) sequences analysed from 95 individuals representing 17 sampling locations scattered through the African miombo (Brachystegia) woodland ecosystem] and phylogeographical statistical procedures (gene genealogy, nested cladistic and admixture proportion analyses), we (i) give a detailed dissection of the geographical genetic structure of Hippotragus niger; (ii) infer the processes and events potentially involved in the population history; and (iii) trace extensive introgressive hybridization in the species. The present-day sable antelope population shows a tripartite pattern of genetic subdivision representing West Tanzanian, Kenya/East Tanzanian and Southern Africa locations. Nested clade analysis revealed that past allopatric fragmentation, caused probably by habitat discontinuities associated with the East African Rift Valley system, together with intermediary episodic long-distance colonization and restricted, recurrent gene flow have played an predominant role in shaping the extent of maternal genetic diversity (10.4%) and population structure. An extensive (average rate of admixture = 20.0%), but geographically circumscribed and unidirectional hybridization event in the past was inferred, resulting in an extreme (the highest discovered so far in mammals) intraspecific difference of 18.2% among morphologically monotypic sable antelopes from West Tanzania. The results are used to provide an evolutionary framework within which taxonomic implications and conservation decisions can be evaluated.     

Assessing Extinction Risk in Small Metapopulations of Golden‐headed Lion Tamarins (Leontopithecus chrysomelas) in Bahia State,Brazil

Golden‐headed lion tamarins (GHLTs; Leontopithecus chrysomelas) are endangered primates endemic to the Brazilian Atlantic Forest, where loss of forest and its connectivity threaten species survival. Understanding the role of habitat availability and configuration on population declines is critical for guiding proactive conservation for this, and other, endangered species. We conducted population viability analysis to assess vulnerability of ten GHLT metapopulations to habitat loss and small population size. Seven metapopulations had a low risk of extirpation (or local extinction) over the next 100 years assuming no further forest loss, and even small populations could persist with immediate protection. Three metapopulations had a moderate/high risk of extirpation, suggesting extinction debt may be evident in parts of the species’ range. When deforestation was assumed to continue at current rates, extirpation risk significantly increased while abundance and genetic diversity decreased for all metapopulations. Extirpation risk was significantly negatively correlated with the size of the largest patch available to metapopulations, underscoring the importance of large habitat patches for species persistence. Finally, we conducted sensitivity analysis using logistic regression, and our results showed that local extinction risk was sensitive to percentage of females breeding, adult female mortality, and dispersal rate and survival; conservation or research programs that target these aspects of the species’ biology/ecology could have a disproportionately important impact on species survival. We stress that efforts to protect populations and tracts of habitat of sufficient size throughout the species’ distribution will be important in the near‐term to protect the species from continuing decline and extinction.     

Mating patterns influence vulnerability to the extinction vortex

Earth's biodiversity is undergoing mass extinction due to anthropogenic compounding of environmental, demographic and genetic stresses. These different stresses can trap populations within a reinforcing feedback loop known as the extinction vortex, in which synergistic pressures build upon one another through time, driving down population viability. Sexual selection, the widespread evolutionary force arising from competition, choice and reproductive variance within animal mating patterns could have vital consequences for population viability and the extinction vortex: (a) if sexual selection reinforces natural selection to fix ‘good genes’ and purge ‘bad genes’, then mating patterns encouraging competition and choice may help protect populations from extinction; (b) by contrast, if mating patterns create load through evolutionary or ecological conflict, then population viability could be further reduced by sexual selection. We test between these opposing theories using replicate populations of the model insect Tribolium castaneum exposed to over 10 years of experimental evolution under monogamous versus polyandrous mating patterns. After a 95‐generation history of divergence in sexual selection, we compared fitness and extinction of monogamous versus polyandrous populations through an experimental extinction vortex comprising 15 generations of cycling environmental and genetic stresses. Results showed that lineages from monogamous evolutionary backgrounds, with limited opportunities for sexual selection, showed rapid declines in fitness and complete extinction through the vortex. By contrast, fitness of populations from the history of polyandry, with stronger opportunities for sexual selection, declined slowly, with 60% of populations surviving by the study end. The three vortex stresses of (a) nutritional deprivation, (b) thermal stress and (c) genetic bottlenecking had similar impacts on fitness declines and extinction risk, with an overall sigmoid decline in survival through time. We therefore reveal sexual selection as an important force behind lineages facing extinction threats, identifying the relevance of natural mating patterns for conservation management.     

Stress and adaptation in conservation genetics

Stress, adaptation and evolution are major concerns in conservation biology. Stresses from pollution, climatic changes, disease etc. may affect population persistence. Further, stress typically occurs when species are placed in captivity. Threatened species are usually managed to conserve their ability to adapt to environmental changes, whilst species in captivity undergo adaptations that are deleterious upon reintroduction into the wild. In model studies using Drosophila melanogaster, we have found that; (a) inbreeding and loss of genetic variation reduced resistance to the stress of disease, (b) extinction rates under inbreeding are elevated by stress, (c) adaptive evolutionary potential in an increasingly stressful environment is reduced in small population, (d) rates of inbreeding are elevated under stressful conditions, (e) genetic adaptation to captivity reduces fitness when populations are reintroduced into the 'wild', and (f) the deleterious effects of adaptation on reintroduction success can be reduced by population fragmentation.