Meta-analysis on the association of population size and life history with inbreeding depression in plants

Inbreeding is common in plants and can have considerable effects on population viability, because of inbreeding depression. Understanding what determines the magnitude of inbreeding depression is of fundamental importance for conservation biology. We used meta-analysis of 116 studies and 107 plant species to investigate the effects of population size, test environment, life history characteristics and stage on the magnitude of inbreeding depression in 13 different fitness traits. We found that inbreeding depression levels significantly increase with population size. This may be a consequence of either, or both, a higher baseline of the level of inbreeding or increased impact of purging in small populations; unfortunately the available data did not allow distinguishing between these potential explanations. In general, inbreeding depression was found to be common across species and environments, and was significant in all traits examined. Yet, the magnitude of inbreeding depression was significantly influenced by plant longevity and life-history stage, and varied depending on how plant fitness was measured. Our findings highlight the fundamental role of population size in influencing the magnitude of inbreeding depression in plants. This clearly has important implications for conservation biology. Moreover, our findings on the overall generality of inbreeding depression confirm that inbreeding depression is one of the key factors reducing plant population fitness and viability. Hence, we need a better understanding on the architecture of inbreeding depression, how different ecological and historical conditions influence the levels of inbreeding depression in natural plant populations, and its impacts on community dynamics.     

Fragmented but not isolated: Contribution of single trees, small patches and long-distance pollen flow to genetic connectivity for Gomortega keule, an endangered Chilean tree

Habitat fragmentation is a major threat to species survival worldwide due to genetic isolation, inbreeding depression, genetic drift and loss of adaptive potential. However the data on how gene-flow changes following habitat fragmentation is contradictory. If there is significant gene-flow between spatially isolated populations then limited conservation resources could be directed away from projects to ‘establish genetic connectivity’ and used to address other consequences of habitat fragmentation.This research focused on an endangered tree species Gomortega keule (Gomortegaceae) in a fragmented landscape in the Central Chile Biodiversity Hotspot and addressed three questions: (1) How far does pollen move between pollen donors and seed trees and what is the shape of the dispersal curve? (2) Do insect pollinators travel outside of forest patches? (3) Do small populations and single trees contribute to genetic connectivity across the landscape?Paternity analysis results show that G. keule’s insect pollinators travel outside of forest patches, over distances of 6 km, beyond the scale of population fragmentation or genetic structure. Pollen moved from small sites and single trees into large sites, as well as in the other direction, indicating these sites play a key role as functioning elements of the wider population and as stepping stones between sites. Fragmentation at the scale investigated has not led to genetic isolation, thus genetic connectivity per se is not a conservation priority. Other consequences of land-use change, specifically continuing habitat loss and population reduction, still threaten the survival of the species.     

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.     

Genetics and extinction

The role of genetic factors in extinction has been a controversial issue, especially since Lande’s paper [Genetics and demography in biological conservation, Science 241 (1988) 1455-1460] paper in Science. Here I review the evidence on the contribution of genetic factors to extinction risk. Inbreeding depression, loss of genetic diversity and mutation accumulation have been hypothesised to increase extinction risk. There is now compelling evidence that inbreeding depression and loss of genetic diversity increase extinction risk in laboratory populations of naturally outbreeding species. There is now clear evidence for inbreeding depression in wild species of naturally outbreeding species and strong grounds from individual case studies and from computer projections for believing that this contributes to extinction risk. Further, most species are not driven to extinction before genetic factors have time to impact. The contributions of mutation accumulation to extinction risk in threatened taxa appear to be small and to require very many generations. Thus, there is now sufficient evidence to regard the controversies regarding the contribution of genetic factors to extinction risk as resolved. If genetic factors are ignored, extinction risk will be underestimated and inappropriate recovery strategies may be used.     

Florida panther dispersal and conservation

We studied dispersal in 27 radio-collared Florida panthers Puma concolor coryi in southern Florida from 1986 to 2000. Male dispersal was longer (mean=68.4 km) than that of females (mean=20.3 km), tended to be circular, frustrated, and of insufficient length to ameliorate inbreeding. Females were philopatric and established home ranges that were less than one home range width away from their natal ranges. All females were successful in establishing territories, whereas males were successful 63% of the time. Dispersing panthers avoided moving toward the southeast and into an area of limited forest cover. Independence and the initiation of dispersal occurred at about 14 months of age and lasted for an average of 7.0-9.6 months for females and males, respectively. On average, Florida panthers disperse shorter distances than are typical for western populations of Puma concolor. A recent increase in long distance male dispersal events may be related to an increase in reproduction and population density resulting from the introduction of female cougars P. c. stanleyana into south Florida. Although the population exhibits the behavioral ability to colonize nearby vacant range, females have yet to do so. Successful dispersal to these areas could be facilitated by habitat restoration and translocation of females.     

Population viability analysis of European bison populations in Polish and Belarusian parts of Bia?owie?a Forest with and without gene exchange

European bison (Bison bonasus) became extinct in the wild at the beginning of the 20th century. The contemporary Lowland line of bison was founded by seven individuals that survived in captivity. The largest population of Lowland bison live in the Bia?owie?a Forest, but the forest and the population are divided by a border fence between Poland and Belarus. This fence is a barrier to the movement of ungulates. In this study, we used population genetic models to predict the future viability of the Polish and Belarusian bison populations. We determined the founder contribution, founder equivalent, mean inbreeding coefficient, mean kinship, and the proportion of genetic diversity retained in the Belarusian bison population. Although the founding group of the Belarusian population was larger than that of the Polish population, the latter had more favourable genetic parameters. We assessed inbreeding depression for fecundity in free-ranging European bison compared to captive individuals. Using population viability analysis (PVA) we modelled both bison populations with or without gene exchange, and with or without incorporating the kinship of the founders. When founder kinship was included, in both populations the mean number of alleles and the gene diversity retained within extant populations decreased substantially compared to PVA models in which founders were not related. The worst genetic parameters were obtained for the Belarusian population under a scenario in which the founders are related and gene exchange is lacking, which is the closest to the real situation. Creation of passages for animals by partial removal of the border fence would have a favourable effect on the genetic variation and viability of both bison populations, especially the Belarusian.     

Polygyny and female breeding failure reduce effective population size in the lekking Gunnison sage-grouse

Populations with small effective sizes are at risk for inbreeding depression and loss of adaptive potential. Variance in reproductive success is one of several factors reducing effective population size (N_e) below the actual population size (N). Here, we investigate the effects of polygynous (skewed) mating and variation in female breeding success on the effective size of a small population of the Gunnison sage-grouse (Centrocercus minimus), a ground nesting bird with a lek mating system. During a two-year field study, we recorded attendance of marked birds at leks, male mating success, the reproductive success of radio-tagged females, and annual survival. We developed simulations to estimate the distribution of male reproductive success. Using these data, we estimated population size () and effective population size N_e for the study population. We also simulated the effects of population size, skewed vs. random mating, and female breeding failure on N_e. In our study population, the standardized variance in seasonal reproductive success was almost as high in females as in males, primarily due to a high rate of nest failure (73%). Estimated N_e (42) was 19% of in our population, below the level at which inbreeding depression is observed in captive breeding studies. A high hatching failure rate (28%) was also consistent with ongoing inbreeding depression. In the simulations, N_e was reduced by skewed male mating success, especially at larger population sizes, and by female breeding failure. Extrapolation of our results suggests that six of the seven extant populations of this species may have effective sizes low enough to induce inbreeding depression and hence that translocations may be needed to supplement genetic diversity.     

The role of genetic mechanisms of sex determination in the survival of small populations of Silene littorea: A reintroduction experiment

Loss of genetic variation in populations may have other effects than inbreeding depression and loss of adaptive potential. In the case of the numerous gynodioecious plant species having cytonuclear systems of sex determination with dominant nuclear restorers of the male function, reduced genetic variation and increased inbreeding would increase the proportion of non-restorer recessive genes found in homozygosity, and therefore that of female plants producing pistillate flowers. This could have opposite effects on the extinction risk of the population. Female plants produce no pollen and may cause pollen limitation, but at the same time they may reduce average homozygosity and inbreeding depression because they are forced outcrossers. We observed that inbreeding indeed increased the frequency of female plants and pistillate flowers in the population, and that this effect was accompanied by reductions in population recruitment independent of inbreeding depression and likely due to pollen limitation. These results suggest that dominant nuclear restorers of pollen production speed up the extinction of small populations of Silene littorea, and that sex determination mechanisms might be an important factor to consider in the conservation of many plant species.     

Genetic diversity and local population structure of fragmented populations of Trillium camschatcense (Trilliaceae)

Trillium camschatcense, a long-lived common woodland herb, has been experiencing intensive habitat fragmentation over the last century in eastern Hokkaido, Japan. We examined the genetic diversity and population genetic structure of 12 fragmented populations with different population sizes using allozyme electrophoresis. The percentage of polymorphic loci and mean number of alleles per locus were positively related to population size, probably due to the stochastic loss of rare alleles (frequency of q<0.1) in small populations. Populations with 350 flowering plants or fewer had lost almost all of their rare alleles. While the heterozygosity and inbreeding coefficient were not related to population size, some small populations showed relatively high inbreeding coefficients. In spite of the low genetic differentiation among overall populations (F_ST=0.130), local population structuring was recognized between the two geographically discontinuous population groups. Within groups, sufficient historical gene flow was inferred, whereas a low dispersal ability of this species and geographical separation could produce apparent differentiation between groups.     

Phenotypic differentiation in fitness related traits between populations of an extremely rare sunflower: Conservation management of isolated populations

Knowledge of the genetic and demographic consequences of rarity is crucial when evaluating the effects of habitat loss and fragmentation on population viability, and for creating management plans in rare plant species. Reduction in population size and in the number of populations can lead to decreased genetic diversity and increased inbreeding. Genetic diversity is often correlated with fitness and is frequently used to identify populations of greatest conservation concern, or those that may be good candidates for ex situ conservation programs. However, an association between these factors is not always clear, and crossing studies evaluating whether there is phenotypic differentiation among populations in fitness related traits can inform managers of suffering populations or good sources for ex situ materials. Crossing studies can also evaluate the potential for genetic rescue to boost fitness in suffering populations. To address these questions, we conducted two generations of controlled crosses between populations of the extremely rare and fragmented sunflower, Helianthus verticillatus. We measured achene viability, germination, survival, and pollen viability (F₁ only) in 176 F₁ and 159 F₂ families. The populations were differentiated with respect to phenotypic fitness measures with one population having significantly lower achene viability and germination. Also, the potential for genetic rescue was observed as gene flow into the less fit population resulted in higher fitness measures in both the F₁ and F₂. Results are discussed with respect to the importance of combining genetic marker data with crosses and the implications for conservation in disjunct populations of rare species.     

Population management of threatened taxa in captivity within their natural ranges: Lessons from Andean bears (Tremarctos ornatus) in Venezuela

Populations of threatened taxa in captivity within their natural ranges can make important contributions to conservation, but these may be compromised by the inappropriate application of population management goals developed in other contexts. We conducted demographic, genetic, and population viability analyses on the captive population of Andean bears (Tremarctos ornatus) in Venezuela to investigate the management of within-range captive populations in general, and to better integrate this population into the conservation of Andean bears in particular. We found that although the present population is very small and not internally self-sustaining, incorporation of confiscated wild individuals has resulted in a low average number of generations in captivity and low inbreeding, with moderate gene diversity and a high probability of future population persistence. However, past imports from extra-range populations have been from over-represented lineages of unknown origin, which have mixed with under-represented Venezuelan ones, reducing the future value of the Venezuelan population as a source for founder stock. Our analyses indicate that the rate of incorporation of wild recruits is a major factor influencing proxy measures of conservation value, and distinguishing within- from extra-range populations. This implies that, contrary to conventional wisdom, internal self-sustainability can be a misguided goal in within-range populations, which furthermore may not be suitable destinations for surplus animals from captive populations elsewhere.     

Inferring seed exchange between farmers from population genetic structure of barley landrace Arabi Aswad from Northern Syria

Apart from their significance in genetic conservation, barley landraces are still favoured by local farmers in low-input farming systems. They often perform more predictably under adverse conditions than modern cultivars due to local adaptation. Increased seed exchange between farmers may put adaptation of local populations of barley landraces at risk. Isozyme markers were used to investigate differentiation and infer gene flow between local populations of barley landrace Arabi Aswad in Northern Syria. Inferred gene flow decreased exponentially with geographic distance and may imply that seed exchange between farmers is limited to a regional scale and diminishes over longer distance. Gene flow seems to be a suitable index for estimating seed exchange in highly inbreeding crop species such as barley. In the future, improved mobility of farmers and extension work may facilitate seed exchange over longer distances, and consequently jeopardise preservation of locally adapted landraces in barley.     

Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances

To preserve populations of endangered bee species, sound knowledge of their maximum foraging distance between nest and host plants is crucial. Previous investigations predicted maximum foraging distances of 100-200 m for small bee species and up to 1100 m for very large species based on mainly indirect methods. The present study applied a new and direct approach to experimentally investigate maximum foraging distances in solitary bees. One endangered and two common species of different body sizes, all of which restrict pollen foraging to a single plant genus, were established in a landscape lacking their specific host plants. Females were forced to collect pollen on potted host plants that were successively placed in increasing distance from fixed nesting stands. The maximum foraging distance recorded for the small Hylaeus punctulatissimus was 1100 m, for the medium sized Chelostoma rapunculi 1275 m and for the large Hoplitis adunca 1400 m, indicating that maximum foraging distances at species level have been underestimated. However, the capability to use resources on such a large spatial scale applied only to a small percentage of individuals as 50% of the females of H. punctulatissimus and H. adunca did not forage at distances longer than 100-225 m and 300 m, respectively. This finding suggests that a close neighbourhood of nesting and foraging habitat within few hundred meters is crucial to maintain populations of these species, and that threshold distances at which half of the population discontinues foraging are a more meaningful parameter for conservation practice than the species specific maximum foraging distances.     

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.     

High levels of hatching failure in an insular population of the South Island robin: a consequence of food limitation?

Endangered birds in insular environments like New Zealand are often translocated to predator-free offshore islands for conservation purposes. Some translocated populations however exhibit reduced fecundity, and it has been suggested that either inbreeding (due to small number of founders) or resource shortages (due to high population density) may limit reproductive success. For example, the South Island robin (Petroica a. australis) population on Motuara Island (59 ha) was founded by only five birds but has increased to ∼600 individuals, or a density >10 times that of the mainland. Despite this apparent success, the rate of hatching failure in this population is three times higher than in mainland populations, with more than a third of eggs failing to hatch. To test if elevated hatching failure is the result of food limitation, we carried out a food supplementation experiment by providing females with mealworms equivalent to ∼50% of their daily energy requirements. Food supplementation had no effect on hatching success, clutch size, incubation attentiveness or nest size. Egg volume increased with food supplementation in one of the two years of this study, but both egg volume and incubation attentiveness were unrelated to rate of hatching failure. As previous genetic analyses confirmed that the bottlenecked population of robins on Motuara Island have significantly less genetic variation than their source population, we conclude that inbreeding depression, and not food limitation, is the most likely explanation for their high rate of hatching failure. We suggest that the experimental translocation of genetically dissimilar individuals be considered as a possible remedy for low productivity in island populations that were initiated with few founders.     

Genetic tracking of the brown bear in northern Pakistan and implications for conservation

Asian bears face major threats due to the impact of human activities as well as a critical lack of knowledge about their status, distribution and needs for survival. Once abundant in northern Pakistan, the Himalayan brown bear (Ursus arctos isabellinus) has been exterminated in most of its former distribution range. It presently occurs sparsely, in small populations, the Deosai National Park supporting the largest isolate. This decline might imply a reduction in genetic diversity, compromising the survival of the population. Using a combination of fecal DNA analysis and field data, our study aimed at assessing the size and genetic status of the Deosai population and give guidelines for its conservation and management. Using fecal genetic analysis, we estimated the population to be 40-50 bears, which compares well with the field census of 38 bears. The northern Pakistani brown bear population may have undergone an approximate 200-300-fold decrease during the last thousand years, probably due to glaciations and the influence of growing human population. However, in spite of the presence of a bottleneck genetic signature, the Deosai population has a moderate level of genetic diversity and is not at immediate risk of inbreeding depression. Gene flow might exist with adjacent populations. We recommend careful monitoring of this population in the future both with field observations and genetic analyses, including sampling of adjacent populations to assess incoming gene flow. The connectivity with adjacent populations in Pakistan and India will be of prime importance for the long-term survival of Deosai bears.     

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.     

Does the acephaline gregarine Monocystis sp. modify the surface behaviour of its earthworm host Lumbricus terrestris?

The earthworm Lumbricus terrestris has relatively low dispersal rates. This can represent a challenge for the internal gregarine parasite Monocystis, the dispersal of which often depends on the host. Mating of Monocystis can also be restricted to parasite stages within the current host individual. Adaptations, including host behavioural modification, that improve parasite transmission and simultaneously avoid inbreeding within a single host individual should be favoured by selection. We used a correlative approach to investigate the question of parasitic manipulation in this Gregarine-Lumbricid system. We observed mature earthworms (n=24) for 3 weeks while recording various measures of activity (surface activity, burrowing activity, surfacing delay, number of surface visits) and correlated parasite load with these activity measures. We found a significant positive correlation between surface activity and midden (or cast) production, which suggests a simple method for assessing the overall activity of local earthworm populations. However, we found no evidence of behavioural manipulation of any measure of host activity. We discuss these results in the context of inbreeding depression and host-parasite coevolution.     

Estimates of minimum viable population sizes for vertebrates and factors influencing those estimates

Population size is a major determinant of extinction risk. However, controversy remains as to how large populations need to be to ensure persistence. It is generally believed that minimum viable population sizes (MVPs) would be highly specific, depending on the environmental and life history characteristics of the species. We used population viability analysis to estimate MVPs for 102 species. We define a minimum viable population size as one with a 99% probability of persistence for 40 generations. The models are comprehensive and include age-structure, catastrophes, demographic stochasticity, environmental stochasticity, and inbreeding depression. The mean and median estimates of MVP were 7316 and 5816 adults, respectively. This is slightly larger than, but in general agreement with, previous estimates of MVP. MVPs did not differ significantly among major taxa, or with latitude or trophic level, but were negatively correlated with population growth rate and positively correlated with the length of the study used to parameterize the model. A doubling of study duration increased the estimated MVP by approximately 67%. The increase in extinction risk is associated with greater temporal variation in population size for models built from longer data sets. Short-term studies consistently underestimate the true variances for demographic parameters in populations. Thus, the lack of long-term studies for endangered species leads to widespread underestimation of extinction risk. The results of our simulations suggest that conservation programs, for wild populations, need to be designed to conserve habitat capable of supporting approximately 7000 adult vertebrates in order to ensure long-term persistence.     

Restricted gene flow in the clonal hepatic Trichocolea tomentella in fragmented landscapes

We studied the genetic diversity, gene flow and population structure among 18 populations of the clonal bryophyte Trichocolea tomentella located in Finland, Lithuania, the UK and Canada using DNA fingerprinting methods. T. tomentella is a habitat-limited, unisexual hepatic, which occupies spring and mesic habitats in woodland. The relatively small populations are increasingly fragmented with a high risk for extinction for extrinsic reasons. The presence of relatively high levels of genetic diversity regardless of population size highlights the role of even small remnant populations as important sources of genetic diversity in T. tomentella. The long-term accumulation of genotypes and somatic mutations may explain the observed levels of diversity. Gene flow among populations seems to be infrequent indicating dispersal limitation also on the relatively small spatial scale. Colonization within populations is not affected by isolation by distance suggesting the occurrence of random short-range dispersal of detached vegetative fragments. The population structure study confirmed the low mortality rates of shoots indicating a long life span of the clones in favourable conditions. Efficient ramet production by branching is likely to operate against interspecific competition. To conclude, T. tomentella appears to persist well in undisturbed habitats due to clonal regeneration, although restricted dispersal capacity is likely to prevent successful (re-)colonization in the potential habitat patches of recovering forest landscapes. The implications of the results for conservation are introduced.