David H. Reed

INBREEDING DEPRESSION INCREASES WITH ENVIRONMENTAL STRESS: AN EXPERIMENTAL STUDY AND META-ANALYSIS

Inbreeding–environment interactions occur when inbreeding leads to differential fitness loss in different environments. Inbred individuals are often more sensitive to environmental stress than are outbred individuals, presumably because stress increases the expression of deleterious recessive alleles or cellular safeguards against stress are pushed beyond the organisms physiological limits. We examined inbreeding–environment interactions, along two environmental axes (temperature and rearing host) that differ in the amount of developmental stress they impose, in the seed‐feeding beetle Callosobruchus maculatus. We found that inbreeding depression (inbreeding load, L) increased with the stressfulness of the environment, with the magnitude of stress explaining as much as 66% of the variation in inbreeding depression. This relationship between L and developmental stress was not explainable by an increase in phenotypic variation in more stressful environments. To examine the generality of this experimental result, we conducted a meta‐analysis of the available data from published studies looking at stress and inbreeding depression. The meta‐analysis confirmed that the effect of the environment on inbreeding depression scales linearly with the magnitude of stress; a population suffers one additional lethal equivalent, on average, for each 30% reduction in fitness induced by the stressful environment. Studies using less‐stressful environments may lack statistical power to detect the small changes in inbreeding depression. That the magnitude of inbreeding depression scales with the magnitude of the stress applied has numerous repercussions for evolutionary and conservation genetics and may invigorate research aimed at finding the causal mechanism involved in such a relationship.

Extinction risk in fragmented habitats

Population models incorporating demographic, environmental and genetic stochasticity were created from long-term data on natural populations of 30 species of vertebrates. The probability of extinction for a single population in a continuous habitat was compared to that of multiple isolated, or semi-isolated, populations occupying a fragmented landscape with an equivalent total carrying capacity. Populations occupying a fragmented landscape were modelled for a range of dispersal rates and levels of asynchrony in the effects of environmental disturbances. Dispersal among subpopulations in the fragmented landscape partially alleviates the effect of fragmentation on extinction rates, despite the models explicitly incorporating disease epidemics which spread between subpopulations through dispersal. Even moderate environmental correlations among subpopulations greatly reduces the viability of the metapopulation relative to the case where the populations are totally independent. Whether a population performed better as a single population or as a metapopulation was strongly affected by the carrying capacity assumed, the time frame examined and the initial fitness of the population. A single population always fared better when the total habitat available was capable of supporting ≤1000 adults. Thus, continued habitat fragmentation can be expected to fuel the ongoing global extinction crisis and conservation efforts should be aimed at interconnecting isolated habitat patches.

The relationship between population size and temporal variability in population size

The relationship between population size and temporal variability in population size was examined using 2387 populations of 203 species from the Global Population Dynamics Database. Population variability, relative to population size, was assayed by regressing the standard deviation of population size against mean population size. Linear regression produced slopes that were less than one in 165 of 203 species. Thus, temporal fluctuations in population size became significantly weaker as population size increased. Similarly, the slope was significantly less than one for a single regression including all 2387 populations, regardless of taxonomic classification. The slopes of the regression lines did not differ for major taxonomic groupings, but the Y-intercept was significantly lower for birds than for the other taxonomic groupings. Factor analysis was used to examine the highly correlated parameters: data reliability, population size and taxonomic lineage. Population size was obviously the most important parameter affecting temporal variation in population size, data reliability was also very important, but taxonomy was of little or no importance. The relationship between temporal variation in population size and mean population size, predicted from the data, was used to predict the probability of extinction assuming a normal distribution of population sizes. This simple model predicts that populations of vertebrates will have to number in the thousands for long-term conservation to be effective.

Inbreeding-stress interactions: evolutionary and conservation consequences.

The effect of environmental stress on the magnitude of inbreeding depression has a long history of intensive study. Inbreeding–stress interactions are of great importance to the viability of populations of conservation concern and have numerous evolutionary ramifications. However, such interactions are controversial. Several meta‐analyses over the last decade, combined with omic studies, have provided considerable insight into the generality of inbreeding–stress interactions, its physiological basis, and have provided the foundation for future studies. In this review, we examine the genetic and physiological mechanisms proposed to explain why inbreeding–stress interactions occur. We specifically examine whether the increase in inbreeding depression with increasing stress could be due to a concomitant increase in phenotypic variation, using a larger data set than any previous study. Phenotypic variation does usually increase with stress, and this increase can explain some of the inbreeding–stress interaction, but it cannot explain all of it. Overall, research suggests that inbreeding–stress interactions can occur via multiple independent channels, though the relative contribution of each of the mechanisms is unknown. To better understand the causes and consequences of inbreeding–stress interactions in natural populations, future research should focus on elucidating the genetic architecture of such interactions and quantifying naturally occurring levels of stress in the wild.

Experimental Evolution of the Genetic Load and its Implications for the Genetic Basis of Inbreeding Depression

Abstract The degree to which, and rapidity with which, inbreeding depression can be purged from a population has important implications for conservation biology, captive breeding practices, and invasive species biology. The degree and rate of purging also informs us regarding the genetic mechanisms underlying inbreeding depression. We examine the evolution of mean survival and inbreeding depression in survival following serial inbreeding in a seed-feeding beetle, Stator limbatus, which shows substantial inbreeding depression at all stages of development. We created two replicate serially inbred populations perpetuated by full-sib matings and paired with outbred controls. The genetic load for the probability that an egg produces an adult was purged at ∼0.45–0.50 lethal equivalents/generation, a reduction of more than half after only three generations of sib-mating. After serial inbreeding we outcrossed all beetles then measured (1) larval survival of outcrossed beetles and (2) inbreeding depression. Survival of outcrossed beetles evolved to be higher in the serially inbred populations for all periods of development. Inbreeding depression and the genetic load were significantly lower in the serially inbred than control populations. Inbreeding depression affecting larval survival of S. limbatus is largely due to recessive deleterious alleles of large effect that can be rapidly purged from a population by serial sib-mating. However, the effectiveness of purging varied among the periods of egg/larval survival and likely varies among other unstudied fitness components. This study presents novel results showing rapid and extensive purging of the genetic load, specifically a reduction of as much as 72% in only three generations of sib-mating. However, the high rate of extinction of inbred lines, despite the lines being reared in a benign laboratory environment, indicates that intentional purging of the genetic load of captive endangered species will not be practical due to high rates of subpopulation extinction.

Inbreeding-environment interactions for fitness: complex relationships between inbreeding depression and temperature stress in a seed-feeding beetle

It is commonly argued that inbred individuals should be more sensitive to environmental stress than are outbred individuals, presumably because stress increases the expression of deleterious recessive alleles. However, the degree to which inbreeding depression is dependent on environmental conditions is not clear. We use two populations of the seed-feeding beetle, Callosobruchus maculatus, to test the hypotheses that (a) inbreeding depression varies among rearing temperatures, (b) inbreeding depression is greatest at the more stressful rearing temperatures, (c) the degree to which high or low temperature is stressful for larval development varies with inbreeding level, and (d) inbreeding depression is positively correlated between different environments. Inbreeding depression (δ) on larval development varied among temperatures (i.e., there was a significant inbreeding-environment interaction). Positive correlations for degree of inbreeding depression were consistently found between all pairs of temperatures, suggesting that at least some loci affected inbreeding depression across all temperatures examined. Despite variation in inbreeding depression among temperatures, inbreeding depression did not increase consistently with our proxy for developmental stress. However, inbreeding changed which environments are benign versus stressful for beetles; although 20°C was not a stressful rearing temperature for outbred beetles, it became the most stressful environment for inbred larvae. The finding that inbreeding-environment interactions can cause normally benign environments to become stressful for inbred populations has important consequences for many areas of evolutionary genetics, artificial breeding (for conservation or food production), and conservation of natural populations.

Genetic effects of habitat fragmentation and population isolation on Etheostoma raneyi (Percidae)

The use of genetic methods to quantify the effects of anthropogenic habitat fragmentation on population structure has become increasingly common. However, in today’s highly fragmented habitats, researchers have sometimes concluded that populations are currently genetically isolated due to habitat fragmentation without testing the possibility that populations were genetically isolated before European settlement. Etheostoma raneyi is a benthic headwater fish restricted to river drainages in northern Mississippi, USA, that has a suite of adaptive traits that correlate with poor dispersal ability. Aquatic habitat within this area has been extensively modified, primarily by flood-control projects, and populations in headwater streams have possibly become genetically isolated from one another. We used microsatellite markers to quantify genetic structure as well as contemporary and historical gene flow across the range of the species. Results indicated that genetically distinct populations exist in each headwater stream analyzed, current gene flow rates are lower than historical rates, most genetic variation is partitioned among populations, and populations in the Yocona River drainage show lower levels of genetic diversity than populations in the Tallahatchie River drainage and other Etheostoma species. All populations have negative FIS scores, of which roughly half are significant relative to Hardy–Weinberg expectations, perhaps due to small population sizes. We conclude that anthropogenic habitat alteration and fragmentation has had a profoundly negative impact on the species by isolating E. raneyi within headwater stream reaches. Further research is needed to inform conservation strategies, but populations in the Yocona River drainage are in dire need of management action. Carefully planned human-mediated dispersal and habitat restoration should be explored as management options across the range of the species.

Spatial and temporal variation in a suite of life-history traits in two species of wolf spider

Abstract 1. Life‐history traits and density were assayed in seven populations of two sympatric species of wolf spider for three consecutive years. The goal of the study was to quantify population dynamics and its relation to spatial and temporal life‐history variation.

Influence of Fruit on Habitat Selection of Asian Bears in a Tropical Forest

ABSTRACT Wild bear populations in Southeast Asia are threatened with extinction, but the ecology and distribution of the 2 species occurring in the regions protected areas is poorly known, so there is little scientific basis underlying conservation strategies. We used bear signs, primarily claw marks on climbed trees, to study habitat selection and distribution of Asiatic black bear (Ursus thibetanus) and sun bear (Helarctos malayanus) across Khao Yai National Park, Thailand from March to December 2008. We found black bear claw marks in 24 of 30 random sample blocks (80%), indicating that this species was widely distributed across Khao Yai. Sun bear signs were much scarcer: their claw marks occurred in 11 blocks (37%); data were too sparse for sun bear so we limited our focus to Asiatic black bear. Using logistic regression, we found that fruit abundance best explained variation in presence of black bear, whereas human disturbance, distance to park edge, elevation, and ground cover had little influence. Fruits appear to be a key resource for Asiatic black bears, and factors affecting fruit abundance or shifts in seasonality (e.g., climate change) will impact bear populations. Knowledge of this relationship will allow managers to be more proactive in managing bears. We recommend using sign surveys for monitoring changes in black bear occupancy as they are inexpensive, efficient, and can be conducted by trained park rangers.

Improving the viability of large-mammal populations by using habitat and landscape models to focus conservation planning

Context. Assessing the viability of animal populations in the wild is difficult or impossible, primarily because of limited data. However, there is an urgent need to develop methods for estimating population sizes and improving the viability of target species. Aims. To define suitable habitat for sambar (Cervus unicolor), banteng (Bos javanicus), gaur (Bos gaurus), Asian elephant (Elephas maximus) and tiger (Panthera tigris) in the Western Forest Complex, Thailand, and to assess their current status as well as estimate how the landscape needs to be managed to maintain viable populations. Methods. The present paper demonstrates a method for combining a rapid ecological assessment, landscape indices, GIS-based wildlife-habitat models, and knowledge of minimum viable population sizes to guide landscape-management decisions and improve conservation outcomes through habitat restoration. Key results. The current viabilities for gaur and elephant are fair, whereas they are poor for tiger and banteng. However, landscape quality outside the current distributions was relatively intact for all species, ranging from moderate to high levels of connectivity. In addition, the population viability for sambar is very good under the current and desired conditions. Conclusions. If managers in this complex wish to upgrade the viabilities of gaur, elephant, tiger and banteng within the next 10 years, park rangers and stakeholders should aim to increase the amount of usable habitat by ~2170 km2 or 17% of existing suitable habitats. The key strategies are to reduce human pressures, enhance ungulate habitats and increase connectivity of suitable habitats outside the current distributions. Implications. The present paper provides a particularly useful method for managers and forest-policy planners for assessing and managing habitat suitability for target wildlife and their population viability in protected-area networks where knowledge of the demographic attributes (e.g. birth and death rates) of wildlife populations are too limited to perform population viability analysis.