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.     

Inbreeding at the edge: does inbreeding depression increase under more stressful conditions?

Edge populations are frequently small and subject to stressful conditions that may compromise their long‐term viability. Inbreeding can play an important role in small populations by reducing genetic diversity, leading to the fixation of deleterious mutations and, finally, carrying populations to an extinction vortex through inbreeding depression. Although stressful conditions may enhance the intensity of inbreeding depression, evidence to date is inconclusive in marginal habitats. Local adaptation, promoting native genotypes, and gene flow, reducing allele fixation, are two factors that can have different effects on the intensity of inbreeding depression. Three populations of Silene ciliata distributed across an elevation gradient at the southernmost edge of the species distribution were used for this study. Several fitness components – germination, survival and growth rate – were compared between inbred seedlings and seedlings from within‐ and between‐population outcrosses, both in the field and controlled conditions. Overall, inbred seedlings had lower fitness than outcrossed seedlings. For most of the variables analysed, similar inbreeding depression effects were found in all three populations, but, for seed weight and seedling survival curve, inbreeding depression was only found in the low altitude population. Similarly, inbreeding depression was more evident in the field than in controlled chamber conditions. Outcrosses between populations contributed to an increase in most fitness estimates and populations, suggesting that the benefits of reducing inbreeding depression overrode the potentially deleterious effects of disrupting local adaptation. Our results suggest that inbreeding depression plays an important role in the fitness of early life stages of Silene ciliata at its southernmost distribution limit, but only provided partial support to the hypothesis that stressful conditions enhance the expression of inbreeding depression.     

Inbreeding and extinction: The effect of environmental stress and lineage

Human activities are simultaneously decreasing the size of wildlife populations (causing inbreeding) and increasing the level of stress that wildlife populations must face. Inbreeding reduces population fitness and increases extinction risk. However, very little information on the impact of stressful environments on extinction risk under inbreeding is available. We evaluated the impact of full sib inbreeding on extinction risk, using Drosophila melanogaster, in a benign and three stressful environments. The three stressful environments involved the addition to the medium of copper sulfate, methanol or alternating copper sulfate and methanol. There were 128 replicate populations for each of the four treatments. Under inbreeding, extinction rates were significantly higher in all three stressful environments compared with the benign environment. The percent extinct at generation eight (F = 0.826) for the four treatments were: 62.5% in the benign environment, 75.8%in the copper sulfate environment, 82.8% in the methanol environment, and 83.6% in the variable stress environment. However, the extinction rate in the variable stress environment did not differ significantly from the constant stress environments. Highly significant differences, among lineages, in extinction risk were detected. The results of this study indicate that wild populations are more vulnerable to inbreeding than indicated by extrapolation from captive environments.     

Does inbreeding affect the extinction risk of small populations?: predictions from Drosophila

A fundamental assumption underlying the importance of genetic risks within conservation biology is that inbreeding increases the extinction probability of populations. Although inbreeding has been shown to have a detrimental impact on individual fitness, its contribution to extinction is still poorly understood. We have studied the consequences of different levels of prior inbreeding for the persistence of small populations using Drosophila melanogaster as a model organism. To this end, we determined the extinction rate of small vial populations differing in the level of inbreeding under both optimal and stress conditions, i.e. high temperature stress and ethanol stress. We show that inbred populations have a significantly higher short‐term probability of extinction than non‐inbred populations, even for low levels of inbreeding, and that the extinction probability increases with increasing inbreeding levels. In addition, we observed that the effects of inbreeding become greatly enhanced under stressful environmental conditions. More importantly, our results show that the impact of environmental stress becomes significantly greater for higher inbreeding levels, demonstrating explicitly that inbreeding and environmental stress are not independent but can act synergistically. These effects seem long lasting as the impact of prior inbreeding was still qualitatively the same after the inbred populations had been expanded to appreciable numbers and maintained as such for approximately 50 generations. Our observations have significant consequences for conservation biology.     

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

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

The effect of selection history on extinction risk during severe environmental change

Environments rarely remain the same over time, and populations are therefore frequently at risk of going extinct when changes are significant enough to reduce fitness. Although many studies have investigated what attributes of the new environments and of the populations experiencing these changes will affect their probability of going extinct, limited work has been directed towards determining the role of population history on the probability of going extinct during severe environmental change. Here, we compare the extinction risk of populations with a history of selection in a benign environment, to populations with a history of selection in one or two stressful environments. We exposed spores and lines of the green alga Chlamydomonas reinhardtii from these three different histories to a range of severe environmental changes. We found that the extinction risk was higher for populations with a history of selection in stressful environments compared to populations with a history of selection in a benign environment. This effect was not due to differences in initial population sizes. Finally, the rates of extinction were highly repeatable within histories, indicating strong historical contingency of extinction risk. Hence, information on the selection history of a population can be used to predict their probability of going extinct during environmental change.     

Genetic rescue and inbreeding depression in Mexican wolves

Although inbreeding can reduce individual fitness and contribute to population extinction, gene flow between inbred but unrelated populations may overcome these effects. Among extant Mexican wolves (Canis lupus baileyi), inbreeding had reduced genetic diversity and potentially lowered fitness, and as a result, three unrelated captive wolf lineages were merged beginning in 1995. We examined the effect of inbreeding and the merging of the founding lineages on three fitness traits in the captive population and on litter size in the reintroduced population. We found little evidence of inbreeding depression among captive wolves of the founding lineages, but large fitness increases, genetic rescue, for all traits examined among F1 offspring of the founding lineages. In addition, we observed strong inbreeding depression among wolves descended from F1 wolves. These results suggest a high load of deleterious alleles in the McBride lineage, the largest of the founding lineages. In the wild, reintroduced population, there were large fitness differences between McBride wolves and wolves with ancestry from two or more lineages, again indicating a genetic rescue. The low litter and pack sizes observed in the wild population are consistent with this genetic load, but it appears that there is still potential to establish vigorous wild populations.     

Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird

There is compelling evidence about the manifest effects of inbreeding depression on individual fitness and populations' risk of extinction. The majority of studies addressing inbreeding depression on wild populations are generally based on indirect measures of inbreeding using neutral markers. However, the study of functional loci, such as genes of the major histocompatibility complex (MHC), is highly recommended. MHC genes constitute an essential component of the immune system of individuals, which is directly related to individual fitness and survival. In this study, we analyse heterozygosity fitness correlations of neutral and adaptive genetic variation (22 microsatellite loci and two loci of the MHC class II, respectively) with the age of recruitment and breeding success of a decimated and geographically isolated population of a long-lived territorial vulture. Our results indicate a negative correlation between neutral genetic diversity and age of recruitment, suggesting that inbreeding may be delaying reproduction. We also found a positive correlation between functional (MHC) genetic diversity and breeding success, together with a specific positive effect of the most frequent pair of cosegregating MHC alleles in the population. Globally, our findings demonstrate that genetic depauperation in small populations has a negative impact on the individual fitness, thus increasing the populations' extinction risk.     

Testing alternative captive breeding strategies with the subsequent release into the wild

We used the housefly (Musca domestica L.) as an experimental model to compare two strategies for the captive breeding of an endangered species: a strategy to minimize inbreeding and balance founder contributions (termed “MAI” for “maximum avoidance of inbreeding”) versus a scheme to select against less fit individuals (disregarding relatedness). By balancing the initial founder contributions, the MAI protocol was analogous to methods for minimizing kinship. In both breeding strategies, the population growth rate was limited to a maximum increase of 50% per generation. Five replicate populations, each starting with five male–female pairs, were subjected to five generations of captive breeding. Six generations of simulated “release into the wild” allowed ad lib breeding with less restrictive population growth potential, in either a benign or stressful environment (i.e., constant or variable temperature). Population size, fecundity, and fertility were assayed throughout the experiment, with juvenile‐to‐adult survival assayed in the second phase of the project. Allozyme assays determined the resultant inbreeding coefficients from the captive breeding schemes. The MAI breeding scheme resulted in significantly lower inbreeding coefficients and higher fitness, with qualitatively reduced extinction potential, most notable in the stressful environment. Spontaneous fitness rebounds suggested that the MAI strategy facilitated some form of purging of inbreeding depression effects. Importantly, the advantages of the MAI strategy were difficult to detect during the captive breeding phase, suggesting that the long‐term advantages of the MAI approach could be underestimated in actual breeding programs. We concur with the common recommendation of maximum avoidance of inbreeding at least for systems with low reproductive potential. Zoo Biol 0:1–18, 2005. © 2005 Wiley‐Liss, Inc.     

Fitness, genetic load and purging in experimental populations of the housefly

The relative effects of purging of the genetic load versus thefixation of deleterious alleles, under inbreeding, will influencea population's probability of extinction. The relative contributionof these two phenomena is expected to depend upon the rate ofinbreeding. A further complication is due to the fact that a purgingof the genetic load in one environment does not necessarily implya purging of the genetic load in other environments. To addressthese two issues, we compare fitness and genetic load in populationsexperiencing similar levels of inbreeding, but occurring as either ashort-term bottleneck or as a consequence of long-term reducedpopulation size, over a range of environments. Inbred populationshave consistently lower fitness than outbred populations acrossall environments tested. However, the bottlenecked populationssuffer less inbreeding depression for a given level of inbreeding,whether or not challenged by novel environments, than populationskept at a constant small size. The results of this study demonstratethat populations initiated from a small number of founders are ableto recover fitness and survive novel environmental challenges,provided that habitat is available for rapid population growth.     

Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population

1. Conservation biologists are concerned about the interactive effects of environmental stress and inbreeding because such interactions could affect the dynamics and extinction risk of small and isolated populations, but few studies have tested for these interactions in nature. 2. We used data from the long-term population study of song sparrows Melospiza melodia on Mandarte Island to examine the joint effects of inbreeding and environmental stress on four fitness traits that are known to be affected by the inbreeding level of adult birds: hatching success, laying date, male mating success and fledgling survival. 3. We found that inbreeding depression interacted with environmental stress to reduce hatching success in the nests of inbred females during periods of rain. 4. For laying date, we found equivocal support for an interaction between parental inbreeding and environmental stress. In this case, however, inbred females experienced less inbreeding depression in more stressful, cooler years. 5. For two other traits, we found no evidence that the strength of inbreeding depression varied with environmental stress. First, mated males fathered fewer nests per season if inbred or if the ratio of males to females in the population was high, but inbreeding depression did not depend on sex ratio. Second, fledglings survived poorly during rainy periods and if their father was inbred, but the effects of paternal inbreeding and rain did not interact. 6. Thus, even for a single species, interactions between the inbreeding level and environmental stress may not occur in all traits affected by inbreeding depression, and interactions that do occur will not always act synergistically to further decrease fitness.     

Inbreeding rate modifies the dynamics of genetic load in small populations

The negative fitness consequences of close inbreeding are widely recognized, but predicting the long-term effects of inbreeding and genetic drift due to limited population size is not straightforward. As the frequency and homozygosity of recessive deleterious alleles increase, selection can remove (purge) them from a population, reducing the genetic load. At the same time, small population size relaxes selection against mildly harmful mutations, which may lead to accumulation of genetic load. The efficiency of purging and the accumulation of mutations both depend on the rate of inbreeding (i.e., population size) and on the nature of mutations. We studied how increasing levels of inbreeding affect offspring production and extinction in experimental Drosophila littoralis populations replicated in two sizes, N = 10 and N = 40. Offspring production and extinction were measured over 25 generations concurrently with a large control population. In the N = 10 populations, offspring production decreased strongly at low levels of inbreeding, then recovered only to show a consistent subsequent decline, suggesting early expression and purging of recessive highly deleterious alleles and subsequent accumulation of mildly harmful mutations. In the N = 40 populations, offspring production declined only after inbreeding reached higher levels, suggesting that inbreeding and genetic drift pose a smaller threat to population fitness when inbreeding is slow. Our results suggest that highly deleterious alleles can be purged in small populations already at low levels of inbreeding, but that purging does not protect the small populations from eventual genetic deterioration and extinction.     

Viral epizootic reveals inbreeding depression in a habitually inbreeding mammal

Inbreeding is typically detrimental to fitness. However, some animal populations are reported to inbreed without incurring inbreeding depression, ostensibly due to past "purging" of deleterious alleles. Challenging this is the position that purging can, at best, only adapt a population to a particular environment; novel selective regimes will always uncover additional inbreeding load. We consider this in a prominent test case: the eusocial naked mole-rat (Heterocephalus glaber), one of the most inbred of all free-living mammals. We investigated factors affecting mortality in a population of naked mole-rats struck by a spontaneous, lethal coronavirus outbreak. In a multivariate model, inbreeding coefficient strongly predicted mortality, with closely inbred mole-rats (F> or = 0.25) over 300% more likely to die than their outbred counterparts. We demonstrate that, contrary to common assertions, strong inbreeding depression is evident in this species. Our results suggest that loss of genetic diversity through inbreeding may render populations vulnerable to local extinction from emerging infectious diseases even when other inbreeding depression symptoms are absent.     

Inbreeding depression for various traits in two cultured populations of the American bay scallop, Argopecten irradians irradians Lamarck (1819) introduced into China

This paper examines the effect of inbreeding level of population on the magnitude of inbreeding depression expressed by comparing them between two cultured populations (A and B) in the hermaphroditic animal of the bay scallop Argopecten irradians irradians. Population A is expected to have less genetic variations and higher inbreeding level due to longer cultured history (20 generations) and less “ancestral” individuals (26 individuals) than population B due to shorter cultured history (4 generations) and more “ancestral” individuals (406 individuals). Two groups within each population were produced, one using self-fertilization and one using mass-mating within the same population. Selfed offspring (AS and BS) from two populations both had lower fitness components than their mass-mated counterparts (AM and BM) and exhibited inbreeding depression for all examined traits, e.g. lower hatching, less viability and slower growth, indicating that inbreeding depression is a common feature in this animal. Fitness components in all traits of offspring from population A significantly differed those from population B and the magnitude of inbreeding depression for all traits in population A with higher inbreeding level was significantly smaller than that in population B with lower inbreeding level, indicating that both fitness components and magnitude of inbreeding depression were significantly affected by inbreeding level of populations and genetic load harbored in population A may be partially purged through inbreeding. Moreover, the magnitude of inbreeding depression in the two populations both varied among traits and life history stages. The present results support the partial-dominance hypothesis of inbreeding depression.     

Trait‐specific consequences of inbreeding on adaptive phenotypic plasticity

Environmental changes may stress organisms and stimulate an adaptive phenotypic response. Effects of inbreeding often interact with the environment and can decrease fitness of inbred individuals exposed to stress more so than that of outbred individuals. Such an interaction may stem from a reduced ability of inbred individuals to respond plastically to environmental stress; however, this hypothesis has rarely been tested. In this study, we mimicked the genetic constitution of natural inbred populations by rearing replicate Drosophila melanogaster populations for 25 generations at a reduced population size (10 individuals). The replicate inbred populations, as well as control populations reared at a population size of 500, were exposed to a benign developmental temperature and two developmental temperatures at the lower and upper margins of their viable range. Flies developed at the three temperatures were assessed for traits known to vary across temperatures, namely abdominal pigmentation, wing size, and wing shape. We found no significant difference in phenotypic plasticity in pigmentation or in wing size between inbred and control populations, but a significantly higher plasticity in wing shape across temperatures in inbred compared to control populations. Given that the norms of reaction for the noninbred control populations are adaptive, we conclude that a reduced ability to induce an adaptive phenotypic response to temperature changes is not a general consequence of inbreeding and thus not a general explanation of inbreeding–environment interaction effects on fitness components.     

Fitness drivers in the threatened Dianthus guliae Janka (Caryophyllaceae): disentangling effects of growth context, maternal influence and inbreeding depression

We studied inbreeding depression, growth context and maternal influence as constraints to fitness in the self-compatible, protandrous Dianthus guliae Janka, a threatened Italian endemic. We performed hand-pollinations to verify outcomes of self- and cross-fertilisation over two generations, and grew inbred and outbred D.?guliae offspring under different conditions - in pots, a common garden and field conditions (with/without nutrient addition). The environment influenced juvenile growth and flowering likelihood/rate, but had little effect on inbreeding depression. Significant interactions among genetic and environmental factors influenced female fertility. Overall, genetic factors strongly affected both early (seed mass, seed germination, early survival) and late (seed/ovule ratio) life-history traits. After the first pollination experiment, we detected higher mortality in the selfed progeny, which is possibly a consequence of inbreeding depression caused by over-expression of early-acting deleterious alleles. The second pollination induced a strong loss of reproductive fitness (seed production, seed mass) in inbred D.?guliae offspring, regardless of the pollination treatment (selfing/crossing); hence, a strong (genetic) maternal influence constrained early life-history traits of the second generation. Based on current knowledge, we conclude that self-compatibility does not prevent the detrimental effects of inbreeding in D.?guliae populations, and may increase the severe extinction risk if out-crossing rates decrease.     

Anthropogenic, ecological and genetic factors in extinction and conservation

Anthropogenic factors constitute the primary deterministic causes of species declines, endangerment and extinction: land development, overexploitation, species translocations and introductions, and pollution. The primary anthropogenic factors produce ecological and genetic effects contributing to extinction risk. Ecological factors include environmental stochasticity, random catastrophes, and metapopulation dynamics (local extinction and colonization) that are intensified by habitat destruction and fragmentation. Genetic factors include hybridization with nonadapted gene pools, and selective breeding and harvesting. In small populations stochastic factors are especially important, including the ecological factors of Allee effect, edge effects, and demographic stochasticity, and the genetic factors of inbreeding depression, loss of genetic variability, and fixation of new deleterious mutations. All factors affecting extinction risk are expressed, and can be evaluated, through their operation on population dynamics.     

Experimental evolution of the genetic load and its implications for the genetic basis of inbreeding depression

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 approximately 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.     

近交衰退:我们检测到了吗

近交衰退产生的原因是近交增加了有害等位基因纯合几率,导致个体适应能力下降。种群变小是导致近交衰退的主要原因,但在实际研究中发现近交衰退并非一定明显表现出来,这可能有以下几个主要的原因遗传负荷的淘汰、在较好的环境下近交衰退会表现不明显、并非能在所有性状中检测到近交衰退、近交衰退只出现在某些发育阶段和不同家系、种群、个体中的近交衰退程度不同。这提示我们近交衰退与生态及遗传密切相关。     

Fitness and adaptation in a novel environment: effect of inbreeding, prior environment, and lineage

Abstract. The ability of populations to undergo adaptive evolution depends on the presence of genetic variation for ecologically important traits. The maintenance of genetic variation may be influenced by many variables, particularly long-term effective population size and the strength and form of selection. The roles of these factors are controversial and there is very little information on their impacts for quantitative characters. The aims of this study were to determine the impacts of population size and variable versus constant prior environmental conditions on fitness and the magnitude of response to selection. Outbred and inbred populations of Drosophila melanogaster were maintained under benign, constant stressful, and variably stressful conditions for seven generations, and then forced to adapt to a novel stress for seven generations. Fitness and adaptability were assayed in each replicate population. Our findings are that: (1) populations inbred in a variable environment were more adaptable than those inbred in a constant environment; (2) populations adapted to a prior stressful environment had greater fitness when reared in a novel stress than those less adapted to stress; (3) inbred populations had lower fitness and were less adaptable than the outbred population they were derived from; and (4) strong lineage effects were detectable across environments in the inbred populations.