Does reduced MHC diversity decrease viability of vertebrate populations?

Loss of genetic variation may render populations more vulnerable to pathogens due to inbreeding depression and depletion of variation in genes responsible for immunity against parasites. Here we review the evidence for the significance of variation in genes of the Major Histocompatibility Complex (MHC) for conservation efforts. MHC molecules present pathogen-derived antigens to the effector cells of the immune system and thus trigger the adaptive immune response. Some MHC genes are the most variable functional genes in the vertebrate genome. Their variation is clearly of adaptive significance and there is considerable evidence that its maintenance is mainly due to balancing selection imposed by pathogens. However, while the evidence for selection shaping MHC variation on the historical timescale is compelling, a correlation between levels of MHC variation and variation at neutral loci is often observed, indicating that on a shorter timescale drift also substantially affects MHC, leading to depletion of MHC diversity. The evidence that the loss of MHC variation negatively affects population survival is so far equivocal and difficult to separate from effects of general inbreeding. Some species with depleted MHC variation seem to be particularly susceptible to infection, but other species thrive and expand following severe bottlenecks that have drastically limited their MHC variation. However, while the latter demonstrate that MHC variation is not always critical for population survival, these species may in fact represent rare examples of survival despite of the loss of MHC variation. There is clearly a compelling need for data that would disclose the possible consequences of MHC diversity for population viability. In particular, we need more data on the impact of MHC allelic richness on the abundance of parasites or prevalence of disease in populations, while controlling for the role of general inbreeding. Before such evidence accumulates, captive breeding programs and other conservation measures aimed at inbreeding avoidance should be favoured over those protecting only MHC variation, especially since inbreeding avoidance programs would usually conserve both types of genetic diversity simultaneously.     

Increased genetic differentiation in house sparrows after a strong population decline: From panmixia towards structure in a common bird

A drastic decline in abundance prompts conservation measures, even though a species may still be common, partly because such a decline may be associated with loss of genetic variability. Longitudinal evidence (i.e. repeated measures across time) for loss of genetic diversity is scarce and mostly concerns organisms that have experienced a severe bottleneck. Here, we study the house sparrow in Finland, where a strong (50–86%) reduction in abundance occurred in four decades, starting earlier and resulting steeper decline in the south than in the north. Based on thirteen polymorphic microsatellites, we compared 12 Finnish populations both prior (mid-1980s) and after (2009) the major population decline. There was no evidence of bottlenecks and only little loss of genetic variation, but we found a significant threefold increase in genetic differentiation (F_ST) across the populations. This may reflect a non-equilibrium situation between the rates of change in the genetic diversity and differentiation and indicate future loss of genetic diversity. Our findings indicate that a strong decline in population size in a relatively common species still leaves a noticeable population-genetic imprint and warrants conservation concern.     

Population clonal diversity and fine-scale genetic structure in <Emphasis Type="Italic">Oryza officinalis</Emphasis> (Poaceae) from China,implications for <Emphasis Type="Italic">in situ</Emphasis> conservation

Population clonal diversity and fine-scale genetic structure of Oryza officinalis Wall. ex Watt, an endangered species in China recently experiencing habitat degradation, was estimated using inter simple sequence repeat markers. We analyzed the genetic variations of 440 samples exhaustively collected from nine O. officinalis populations. Relatively rich clonal diversity and poor genetic variation were found in the extant populations. We found that the number of genets, the percentage of polymorphic loci, and gene diversity decreased with population decline, suggesting that habitat degradation will lead to further genetic depletion of O. officinalis populations. A pronounced spatial genetic structure occurs at both the ramet and genet levels in several larger populations, which is the result of clonal growth and concomitant inbreeding. The in situ conserved population PS holds much more genotypes than other populations with the similar population size, which might have more seedling recruitments from the soil seed bank due to habitat disturbance, suggesting a moderate disturbance combined with habitat degradation-avoiding measures are effective for in situ conservation of this species.     

Low impact of present and historical landscape configuration on the genetics of fragmented Anthyllis vulneraria populations

Decreasing habitat fragment area and increasing isolation may cause loss of plant population genetic diversity and increased genetic differentiation between populations. We studied the relation between the historical and the present landscape configuration (i.e., patch area and patch connectivity), and the present management of calcareous grassland fragments on the one hand, and the within and between population genetic structure of 18 Anthyllis vulneraria populations on the other hand. Despite the long-time fragmentation history and the mainly selfing breeding system of the species, we detected very low genetic differentiation (Φ_st = 0.056) among habitat fragments and no significant isolation-by-distance relation. Average within fragment genetic diversity measured as molecular variance and expected heterozygosity, were relatively high (16.46 and 0.28, respectively), and weakly positively correlated with the current fragment area, most likely because larger fragments contained larger populations. We found no effects of the historical landscape configuration on the genetic diversity of the populations. Our data suggest that the consequences of habitat fragmentation for genetic differentiation and genetic diversity of A. vulneraria are relatively minor which is very likely due to the historical high levels of seed exchange among fragments through grazing and roaming livestock. This study provides indirect evidence that nature management by grazing not only positively affects habitat quality but that it might also mitigate the genetic consequences of habitat fragmentation. From the conservation point of view, this study illustrates the importance of grazing and of the regular transport of livestock between fragments to prevent the long-term effects of fragmentation on the genetic diversity of the populations studied.     

Do species life history traits explain population responses to roads? A meta-analysis

Efforts to mitigate road effects are now common in new highway construction projects. For effective mitigation of road effects it is important to identify the species whose populations are reduced by roads, so that mitigation efforts can be tailored to those species. We conducted a meta-analysis using data from 75 studies that quantified the relationship between roads and/or traffic and population abundance of at least one species to determine species life history characteristics and behavioral responses to roads and/or traffic that make species or species groups prone to negative road and/or traffic effects. We found that larger mammal species with lower reproductive rates, and greater mobilities, were more susceptible to negative road effects. In addition, more mobile birds were more susceptible to negative road and/or traffic effects than less mobile birds. Amphibians and reptiles were generally vulnerable to negative road effects, and anurans (frogs and toads) with lower reproductive rates, smaller body sizes, and younger ages at sexual maturity were more negatively affected by roads and/or traffic. Species that either do not avoid roads or are disturbed by traffic were more vulnerable to negative population-level effects of roads than species that avoid roads and are not disturbed by traffic. In general, our results imply that priority for mitigation should be directed towards wide-ranging large mammals with low reproductive rates, birds with larger territories, all amphibians and reptiles, and species that do not avoid roads or are disturbed by traffic.     

The responses of leaf litter invertebrates to environmental gradients along road edges in subtropical island forests

Knowledge of how roads affect forest biodiversity can be improved by measuring the responses of indicator species to complex environmental gradients caused by these infrastructures. We studied litter invertebrate species responses to road edges in laurel and pine forests in Tenerife, Canary Islands. We sampled invertebrates from litter and assessed the environmental variation related to road proximity. We also assessed the effect of relevant environmental predictors on a diverse array of potential indicator species. We applied canonical ordination and non-parametric regression (Lowess) to classify invertebrate species responses to roads and their associated gradients. Three types of responses to road edge proximity were defined for the most common invertebrate taxa: edge-preferring or edge specialists, interior-preferring or edge-avoiders, and edge-indifferent or neutral species. Those species appearing most frequently and with higher population density between 1 and 20 m from the edge (commonly peaking at 10 m from the road) were categorized as edge-preferring. We classified taxa attaining peak population densities at or beyond 60 m from the edge (and most commonly 100 m) as interior species. Edge-neutral species were those without an evident pattern of stabilization in abundance along the gradient and with peaks in abundance at varying distance intervals. These edge litter communities contain a high native and endemic diversity but also a significant density of alien fauna. The specific patterns of penetration of road edge effects on invertebrate species should be seen as having a pervasive and cumulative impact considering the exceptionally large number of roads in these forests and the high population densities of alien invertebrates. Future management plans for forest conservation on the Canary Islands should include the highly altered but valuable litter communities along road edges.     

Influence of forest fragmentation on an endangered large-bodied lemur in northwestern Madagascar

Madagascar’s diverse and mostly endemic fauna and flora suffer from recent landscape changes that are primarily caused by high levels of human activities. The loss and fragmentation of forest habitats are well known consequences of human activities. In this study, we investigate the effects of forest fragmentation on presence, abundance and genetic diversity in a larger-bodied lemur species, Lepilemur edwardsi, in northwestern Madagascar. In addition, we characterized the genetic differentiation among populations and demographic changes. We found L. edwardsi at only 13 (76.5%) of 17 visited sites, 11 of which were situated in the Ankarafantsika National Park (ANP). We captured between two and 17 individuals per site. We sequenced the mtDNA d-loop of all samples and genotyped 14 microsatellite loci in two exemplary populations for demographic analyses. A negative influence on forest fragmentation could be detected, since the fragments had a lower genetic diversity than sites in the ANP. Genetic differentiation between populations ranged from low to high but was almost always significant. A typical pattern of isolation-by-distance could not be detected and the data could rather be interpreted as results of random genetic drift. The data furthermore revealed signals of a demographic collapse of about two orders of magnitude in the two exemplary sites. This decline probably started during the last few hundred years of intensified human disturbances and population growth. Given the results of this study, urgent conservation actions are needed and should concentrate on an effective protection of the few remaining populations in order to ensure the long-term survival of L. edwardsi.     

Decline of an isolated timber rattlesnake (Crotalus horridus) population: Interactions between climate change, disease, and loss of genetic diversity

Extinction of populations from anthropogenic forces rarely has a single cause. Instead, population declines result from a variety of factors, including habitat loss, inbreeding depression, disease, and climate change. These impacts often have synergistic effects that can lead to rapid decline in isolated populations, but case studies documenting such processes are rare. Here, we describe the recent decline of the last known population of timber rattlesnakes (Crotalus horridus) in the state of New Hampshire. We used polymorphic nuclear DNA markers to compare genetic diversity of this population to other populations in the region that are not isolated. We also compare results from ongoing field monitoring of these populations. Genetic analyses reveal that the New Hampshire population lacks genetic diversity and exhibits signs of a recent bottleneck. New Hampshire snakes also exhibited high levels of morphological abnormalities (unique piebald coloration, amelanistic tongues) indicative of inbreeding depression. Furthermore, after a year with exceptionally high summer rainfall, a skin infection of unknown etiology caused significant mortality in the New Hampshire population, whereas other surveyed non-inbred populations were unaffected. This case study demonstrates how different anthropogenic impacts on natural environments can interact in unexpected ways to drive threatened populations toward extinction.     

Restricted gene flow and genetic drift in recently fragmented populations of an endangered steppe bird

Identifying the genetic processes derived from habitat fragmentation is critical for the conservation of endangered species. We conducted an integrated analysis of genetic patterns in the endangered Dupont’s lark (Chersophilus duponti), a circum-Mediterranean songbird threatened by the loss and fragmentation of natural steppes in recent decades. After sampling all the remaining Spanish populations and the two closest North African ones, we found that the Mediterranean Sea acts as a major barrier against gene flow and that recent habitat fragmentation is isolating Spanish populations at different spatial scales. While we found a historical signal of gene flow among Spanish regions, a coalescent model supported that the ancestral panmictic population is evolving into several different units in the absence of current gene flow, genetic drift being more intense in the smaller and more isolated populations. Moreover, small-scale spatial autocorrelation analyses showed that genetic differentiation is also acting within populations. The spatial genetic structure, significant levels of inbreeding and high relatedness within patches raise concerns on the viability of most of the extant populations. We highlight the urgency for steppe patches to be protected, expanded and reconnected, considering the genetic clusters identified here rather than the previously considered eco-geographic regions occupied by the species. Meanwhile, translocations could be considered as a complementary, faster management action to attenuate the crowding and genetic effects of population fragmentation and the extinction risk of small populations without compromising the current local adaptations, culture diversity and genetic clusters already known for the species.     

Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest

Tropical rainforests are becoming increasingly fragmented and understanding the genetic consequences of fragmentation is crucial for conservation of their flora and fauna. We examined populations of the toad Rhinella ornata, a species endemic to Atlantic Coastal Forest in Brazil, and compared genetic diversity among small and medium forest fragments that were either isolated or connected to large forest areas by corridors. Genetic differentiation, as measured by F_ST, was not related to geographic distance among study sites and the size of the fragments did not significantly alter patterns of genetic connectivity. However, population genetic diversity was positively related to fragment size, thus haplotype diversity was lowest in the smallest fragments, likely due to decreases in population sizes. Spatial analyses of genetic discontinuities among groups of populations showed a higher proportion of barriers to gene flow among small and medium fragments than between populations in continuous forest. Our results underscore that even species with relatively high dispersal capacities may, over time, suffer the negative genetic effects of fragmentation, possibly leading to reduced fitness of population and cases of localized extinction.     

Identifying road mortality threat at multiple spatial scales for semi-aquatic turtles

Prioritizing sites for localized mitigation measures, and forecasting the effect of interventions on an endangered population, requires an understanding of the spatial scales at which threat processes operate. Road mortality is among the greatest threats to semi-terrestrial freshwater turtles due to the group’s life-history traits. Declining throughout much of their range, spotted (Clemmys guttata) and Blanding’s turtles (Emydoidea blandingii) are exposed to high road densities and traffic volumes in the northeastern United States. We examine the distribution of roadkill risk for spotted and Blanding’s turtles at three spatial scales. Tortuosity during upland movements was used to predict road-crossing locations at the single-movement scale. A gravity model of wetland-to-wetland interactions was then developed to identify road mortality hot spots at a broader road segment scale. Finally, road-crossing risk was assessed at the scale of focal areas that support distinct populations, using a population viability analysis to evaluate the consequences of road mortality on resident populations. The observed spatial variability of road mortality risk was high for single road crossing movements, limiting the effectiveness of static mitigation measures conducted at this scale. At the broader road segment scale, road mortality hotspots were evident. The demographic risk associated with roads varied widely among discrete populations, with probabilities of extinction over 100-year projections reaching 5.1% for spotted turtles, and 58.8% for Blanding’s turtles. We conclude that conservation interventions are most likely to be effective in mitigating the effects of road mortality when implemented at the road segment and population scales.     

Reduced effective population size in an overexploited population of the Nile crocodile (Crocodylus niloticus)

Unchecked exploitation of wildlife resources is one of the major factors influencing species persistence throughout the world today. A significant consequence of exploitation is the increasing rate at which genetic diversity is lost as populations decline. Recent studies suggest that life history traits affecting population growth, particularly in long-lived species, may act to moderate the impact of population decline on genetic variation and lead to remnant populations that appear genetically diverse despite having passed through substantial demographic bottlenecks. In this study we show that the retention of genetic variation in a partially recovered population of Nile crocodile is deceptive, as it masks the reality of a significant decline in the population’s effective size (N_e). Repeated episodes of unchecked hunting in the mid to late 20th century have today led to a five-fold decrease in the population’s N_e. Using current census data we estimate the contemporary N_e/N ratio as 0.05 and, in light of quotas that permit the ongoing removal of adults, simulated the likely effects of genetic drift on extant levels of variation. Results indicate that even if the current effective size is maintained, both allelic diversity and heterozygosity will decline. Our findings have complex implications for long-lived species; an emphasis on the retention of genetic variation alone, whilst disregarding the effects of population decline on effective size, may ultimately obscure the continued decline and extinction of exploited populations.     

Integrating demographic and genetic approaches in plant conservation

We summarize the problems that populations of formerly common plants may encounter when habitat fragmentation isolates them and reduces population size. Genetic erosion, inbreeding depression, Allee-effects on reproductive success, catastrophes and environmental stochasticity are illustrated with studies on species that have recently become rare in The Netherlands due to habitat fragmentation. These clearly indicate that population viability is negatively affected. We also show that in the recent literature (since 1980), most studies on the conservation of rare plants have addressed population genetic structure and relationships between genetic variation and population size. Though important, these studies are not suitable for assessing the importance of genetics for population viability. In turn, demographic studies can detect changes in vital rates in small populations, but cannot reveal underlying genetic causes. Fitness and demographic studies are also well-represented in the literature, but remarkably few studies have attempted to integrate empirical demographic and genetic studies. We discuss two approaches to fill this very important lacuna in our knowledge. One of these constructs matrix-projection models on the basis of demographic censuses of—if possible—large and viable populations, and combines these with the results of experiments to determine inbreeding effects on demographic transitions and, subsequently, population growth and extinction. The other approach is to demographically monitor experimentally created small and large populations with low and high genetic variation and measure their actual growth rates and probabilities of extinction. We conclude that demography and demographic-genetic experiments should play a central role in plant conservation genetics.     

Low levels of genetic variation among southern peripheral populations of the threatened herb, Leontice microrhyncha (Berberidaceae) in Korea

Levels of genetic variation and intrapopulation genetic structures of Leontice microrhyncha S. Moore (Berberidaceae) were assessed for six populations in South Korea, representing the southern most range of a species found in Northeast China and the Korean peninsula. Detected genetic diversity (H_es) was very low (0.024) and F_IS values showed large heterozygote deficiencies. The small percentage of polymorphic loci and numbers of alleles per locus suggest that L. microrhyncha has a history of severe or long-lasting population bottlenecks that have eroded genetic diversity. This study suggests that the Korean population appears to consist of two historically isolated and independently evolving populations. It seems likely that these groups have been isolated and unstable for a significant period of time. However, the effects of recent habitat fragmentation on the historically disjunct and fragmented population system found in L. microrhyncha were not those predicted from the lack of significant relationships between population-level patterns of genetic variation and population sizes. Most non-unique genotypes were shared by most individuals and the lower level of diversity, high levels of inbreeding and population differentiation as well as high rate of seed production indicated that this species is autogamous and self-compatible and probably largely selfing. Therefore, to preserve extant genetic variation, all populations must be protected across the small geographic range of the species to retain both allelic and genotypic diversity.     

Conservation genetics of evolutionary lineages of the endangered mountain yellow-legged frog, Rana muscosa (Amphibia: Ranidae), in southern California

Severe population declines led to the listing of southern California Rana muscosa (Ranidae) as endangered in 2002. Nine small populations inhabit watersheds in three isolated mountain ranges, the San Gabriel, San Bernardino and San Jacinto. One population from the Dark Canyon tributary in the San Jacinto Mountains has been used to establish a captive breeding population at the San Diego Zoo Institute for Conservation Research. Because these populations may still be declining, it is critical to gather information on how genetic variation is structured in these populations and what historical inter-population connectivity existed between populations. Additionally, it is not clear whether these populations are rapidly losing genetic diversity due to population bottlenecks. Using mitochondrial and microsatellite data, we examine patterns of genetic variation in southern California and one of the last remaining populations of R. muscosa in the southern Sierra Nevada. We find low levels of genetic variation within each population and evidence of genetic bottlenecks. Additionally, substantial population structure is evident, suggesting a high degree of historical isolation within and between mountain ranges. Based on estimates from a multi-population isolation with migration analysis, these populations diversified during glacial episodes of the Pleistocene, with little gene flow during population divergence. Our data demonstrate that unique evolutionary lineages of R. muscosa occupy each mountain range in southern California and should be managed separately. The captive breeding program at Dark Canyon is promising, although mitigating the loss of neutral genetic diversity relative to the natural population might require additional breeding frogs.     

Climate change is linked to long-term decline in a stream salamander

Amphibian declines have been documented worldwide and several have been linked to climate change, but the long-term data needed to detect declines are largely restricted to pond-breeding species. This limits our knowledge of population trends in other major groups of amphibians, including stream salamanders, which have their greatest diversity in North America. I hypothesized that increasing air temperature and precipitation in northeastern North America caused abundance of the stream salamander Gyrinophilus porphyriticus in a New Hampshire population to decline between 1999 and 2010. I found a significant decline in abundance of G. porphyriticus adults over this 12-year period, and no trend in larval abundance. Adult abundance was negatively related to annual precipitation, which is predicted to increase further in the Northeast due to climate change. Analysis of a 6-year capture–mark–recapture data set for the same population showed no temporal variation in larval and adult detectability, validating the abundance data, and no variation in larval and adult survival. However, survival during metamorphosis from the larval to adult stage declined dramatically. These results suggest that increasing precipitation is causing a decline in adult recruitment, which, if it persists, will lead to local extinction. A likely mechanism for the decline in adult recruitment is mortality of metamorphosing individuals during spring and fall floods, which have increased in volume and frequency with the increase in precipitation. More broadly, this study presents strong evidence that the amphibian decline crisis extends to North America’s stream salamanders, and shows the critical need to collect population data on these species.     

Landscape evaluation of female black bear habitat effectiveness and capability in the North Cascades, Washington

We used logistic regression to derive scaled resource selection functions (RSFs) for female black bears at two study areas in the North Cascades Mountains. We tested the hypothesis that the influence of roads would result in potential habitat effectiveness (RSFs without the influence of roads) being greater than realized habitat effectiveness (RSFs with roads). Roads consistently had a negative influence on black bear RSFs across seasons and study areas. Roads reduced habitat effectiveness during all seasons at both study areas and changes in the potential habitat values ranged from 1.7% to 16.9%. The greatest reduction in habitat values occurred during the early-season on the west-side study area due to high open road densities. These results support the hypothesis that roads reduce habitat effectiveness for black bears. The influence of roads could be reduced through road closures to reduce open road densities and limit traffic volumes. We then used the scaled RSFs in a habitat-based population model to assess the influences of timber harvest and roads on potential black bear population sizes. On the west-side study area the potential black bear population size was most influenced by moderate use roads and timber harvest during the early-season (41% reduction). On the east-side study area, low use roads had the greatest effect on potential black bear population during the early-season (10% reduction). During the late-season, in both study areas, roads had less influence on the potential population sizes as bears were able to access habitats away from roads. The habitat-population model provided reasonable estimates of bear densities compared to other study areas with similar habitats and could be extrapolated to estimate potential black bear populations in other areas with similar habitats. This approach may provide a useful link between the landscape ecology and population biology of black bears, and could eventually be useful in the development of habitat-based population viability analyses.     

湖南典型茶树地理种群遗传多样性研究

本文利用RAPD分子标记技术，对4个湖南典型茶树地理种群的240个单株的遗传多样性、种群内和种群间的遗传变异进行研究，结果表明：21个10碱基随机引物共检测到226条谱带，其中多态性谱带为201条，占88.9%。遗传多样性分析结果显示：Shannon's多样性指数为0.43，74.7%的变异分布于群体内，而种群间变异占了25.3%；Nei's指数群体总基因多样度(HT)为0.37，群体内平均基因多样度(HS)0.28，群体间的基因多样度(HST)0.09，群体Nei's基因分化系数（GST）为0.23，说明76.7%的变异存在于种群间，群体内的变异占了总变异的23.3%，与Shannon's多样性指数相比基本一致，均表明种群内有较丰富的遗传变异；种群间的基因流（Nm）为0.74，显示种群间的基因交流有限。     

Quantitative variation as a tool for detecting human-induced impacts on genetic diversity

We propose quantitative genetic variation as a useful tool complementary to molecular variation in order to detect changes in biodiversity caused by different human-induced activities. We simulated a metapopulation setting under a number of realistic scenarios caused by anthropogenic activities (population isolation, reduced carrying capacity or reproductive rates, shifts in the local optima, and enhanced environmental variation or mutational rates). The effects on diversity of these scenarios were assessed for neutral variation estimated from molecular markers and for an additive quantitative trait that represents a typical morphological characteristic subject to stabilising selection promoting local adaptation to environmental conditions. The results show that monitoring quantitative genetic variation can be more informative than neutral variation to detect some human-induced environmental or genetic impacts on diversity, both at intra and interpopulation levels. We also compared the precision of diversity estimates obtained from molecular markers and quantitative traits. Under low migration rates and typical selection intensities for the quantitative trait, the precision of estimates can be substantially larger for a quantitative trait than for a single molecular marker. Thus, about 10-20 (2-4) independent markers are necessary for the precision of estimates of heterozygosity (population differentiation) from molecular markers to reach that of genetic variances (differentiation) from quantitative traits.