Article

Unexpected positive and negative effects of continuing inbreeding in one of the world's most inbred wild animals

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  • U.S. Geological Survey
Article

Unexpected positive and negative effects of continuing inbreeding in one of the world's most inbred wild animals

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Abstract

Inbreeding depression, the reduced fitness of offspring of related individuals, is a central theme in evolutionary biology. Inbreeding effects are influenced by the genetic makeup of a population, which is driven by any history of genetic bottlenecks and genetic drift. The Chatham Island black robin represents a case of extreme inbreeding following two severe population bottlenecks. We tested whether inbreeding measured by a 20-year pedigree predicted variation in fitness among individuals, despite the high mean level of inbreeding and low genetic diversity in this species. We found that paternal and maternal inbreeding reduced fledgling survival and individual inbreeding reduced juvenile survival, indicating that inbreeding depression affects even this highly inbred population. Close inbreeding also reduced survival for fledglings with less-inbred mothers, but unexpectedly improved survival for fledglings with highly inbred mothers. This counterintuitive interaction could not be explained by various potentially confounding variables. We propose a genetic mechanism, whereby a highly inbred chick with a highly inbred parent inherits a "proven" genotype and thus experiences a fitness advantage, which could explain the interaction. The positive and negative effects we found emphasize that continuing inbreeding can have important effects on individual fitness, even in populations that are already highly inbred. This article is protected by copyright. All rights reserved.

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... Regular storm events and strong winds coupled with an aversion to flying across open areas prevent the robin from flying the 11 km distance between the two islands it inhabits, with no evidence of natural dispersal since the Rangatira population was established in the 1980s (Kennedy 2009 Although the recovery of the black robin population demonstrated that even species on the brink of extinction can be saved, in the first ten years following the bottleneck severe inbreeding took place with frequent brother-sister and father-daughter matings (Massaro et al. 2013a). These high rates of inbreeding had impacts on population fitness, whereby juvenile survival is reduced and there is no evidence of purging (Kennedy et al. 2014;Weiser et al. 2016). A previous study of black robin genetics found the black robin exhibited low minisatellite diversity (Ardern & Lambert 1997). ...
... I will also investigate whether there is population substructuring within the larger Rangatira black robin population. Several studies identify two distinct populations on Rangatira Island, one in the northern Woolshed Bush, and a second in the more southern Top Bush, and present separate analyses for each (Kennedy et al. 2014;Weiser et al. 2016). However, dispersal between these patches has been recorded (M. ...
... This reduction in fitness is known as inbreeding depression, and can affect fitness traits at all life stages (Charlesworth & Charlesworth 1999;Grueber et al. 2010;Keller & Waller 2002;Wright et al. 2008). (Ardern & Lambert 1997) may have contributed to increase population vulnerability, as some individuals are estimated to have inbreeding coefficients that are higher than those in selfing populations (Kennedy et al. 2014;Weiser et al. 2016). ...
Thesis
Full-text available
Endemic island populations worldwide are at greater risk of extinction than similar mainland populations, in part due to the specific genetic threats faced by small populations, namely of loss of genetic diversity and inbreeding. Reduced genetic diversity limits the ability of populations to adapt to altered conditions, while unavoidable inbreeding reduces population fitness through the effects of inbreeding depression. Effective conservation management requires the understanding of these effects on populations of interest to adopt appropriate strategies to reduce such threats, and thereby ensure long-term population persistence. Through the use of next-generation sequencing, I isolated 11 polymorphic microsatellite loci to allow analysis of current levels of genetic diversity in the endangered Chatham Island black robin Petroica traversi. The black robin has a history of small population size, including a population bottleneck of a single breeding pair, prior to recovery of population size over the past 30 years. The species is currently limited to populations on two small islands, and likely has a high extinction risk due to unavoidable inbreeding in the recovering populations, and may have experienced loss of genetic diversity due to strong genetic drift within these small populations. I compared levels of genetic diversity in the black robin to that of its closest congener, the Chatham Island tomtit Petroica macrocephala chathamensis, to assess how the population history of the black robin has affected its genetic diversity. Additionally, I compared levels of diversity between island populations of each species, to determine whether the smaller populations experienced lower diversity and therefore greater extinction vulnerability. Genetic diversity was lower in the black robin than the tomtit, and lower in the smaller populations of both species. The detection of levels of genetic diversity in the tomtit similar to those of threatened species suggests population viability of this species of least concern may be lower than expected. The two island populations of black robin are thought to have been isolated from one another for 26 years, and so populations were genotyped to determine whether this isolation has resulted in population differentiation, despite the short period of isolation. The two populations show substantial genetic differentiation, indicating genetic drift has had strong independent effects on these isolated populations. Although the tomtit exists on three islands, there was no evidence of current dispersal between the two populations assessed, and there was a similar level of differentiation between these populations and the black robin populations. Over 30 years of observational data show the black robin to be socially monogamous, with no evidence of extra-pair breeding. However, assessment of the social pedigree using microsatellite genotyping found a conservative rate of extra-pair paternity of approximately 14%, and the existence of a low-level of intraspecific brood paternity could not be rejected. As yet, the reason for the evolution of a strategy of extra-pair paternity is unknown. From the results of this study, I recommend reciprocal translocations of black robins between island populations as a form of assisted gene flow to bolster genetic diversity of each population, and to reduce inbreeding in the smaller of the two populations. Furthermore, the establishment of a third population is recommended to minimise extinction vulnerability of this endangered species. As the black robin is not genetically monogamous, selection of individuals for translocation will require the use of molecular techniques to assess relatedness, rather than the social pedigree, to maximise success.
... Our previous analysis of inbreeding effects in sand lizards show that different developmental stages may be differently affected by inbreeding so that incubation is a more susceptible stage with more inbreeding effects than first year survival in the wild (Bererhi et al., 2019). In spite of the loss of genetic diversity, on rare occasions inbreeding has positive fitness effects due to purging of deleterious recessive alleles (Helgason et al., 2008) or because of local adaptation of specific genotypes (the 'proven genotype' hypothesis; Weiser et al., 2016). This is best exemplified by the black robin or Chatham Island robin (Petroica traversi), an endangered bird from the Chatham Islands off the east coast of New Zealand. ...
... Paternal and maternal inbreeding reduced fledgling survival and individual inbreeding reduced juvenile survival, indicating that inbreeding depression affects even this highly inbred population. Close inbreeding also reduced survival for fledglings with less-inbred mothers, but unexpectedly improved survival for fledglings with highly inbred mothers (Weiser et al., 2016). In our own work, we also showed that parental effects per se, regardless of inbreeding, had significant effects on offspring viability in early developmental stages (Bererhi et al., 2019). ...
Article
Loss of genetic variation is an increasing problem in many natural populations as a result of population fragmentation, inbreeding, and genetic drift, which may lead to inbreeding depression and subsequent “extinction vortices”. In such cases, outbreeding offers a potential population saviour from extinction. Here we compare offspring viability between an experimentally founded outbred island population of sand lizards Lacerta agilis, and an inbred mainland source population on the Swedish West coast. We have studied the mainland population for over a decade during which >4000 offspring from >500 parents were monitored. We conducted an outbreeding experiment in which lizards from the mainland population with relatively low genetic variation were crossbred with lizards from distant populations that lack gene flow. The resulting 454 offspring were introduced to an otherwise uninhabited island with ideal sand lizard habitat. A survey of the island two decades later showed that offspring produced by females from the experimentally founded population had 13% higher hatching success (99.3% versus 86.4%) and elimination of the malformations occurring in 21% of clutches in the mainland source population. These results co-occur with higher genetic diversity. We conclude that outbreeding improved offspring viability in our island population ca 5–6 generations after the founding event, that is, with sustained viability effects at a time when heterotic effects are expected to have subsided.
... On Rangatira Island, the black robin is hypothesised to exist in two populations, each inhabiting a distinct bush area; Woolshed Bush to the north, and Top Bush to the south, separated by Skua Gully (Kennedy 2009;Weiser et al. 2016). Dispersal may have been limited between forest patches (Butler and Merton 1992;Kennedy 2009), and so there may be some level of differentiation between robins in these two distinct habitat areas. ...
... Two recent studies (Kennedy et al. 2014;Weiser et al. 2016) have treated the Rangatira population as two separate populations inhabiting different forested areas. We found there is a lack of evidence for genetic differentiation between the two forest populations. ...
Article
Full-text available
Small island populations are particularly prone to extinction due to the effects of genetic drift and inbreeding reducing genetic variation and fitness of such populations. Furthermore, isolated island populations may experience population divergence due to drift or divergent selection. Reciprocal translocations of individuals between populations may be used to stimulate gene flow between such isolated populations. To determine whether populations of the endangered Chatham Island black robin Petroica traversi may benefit from such translocations, we compared levels of genetic diversity and differentiation within and among populations of the black robin and its sympatric sister-species, the Chatham Island tomtit Petroica macrocephala chathamensis. Although the black robin has recovered following a severe population bottleneck, the bottleneck and subsequent intense inbreeding experienced by the black robin have likely had long-term consequences affecting the viability of this endangered species. We analysed the genetic diversity and population structure of the black robin at 15 polymorphic microsatellite loci, and compared this to the level and pattern of genetic diversity from 17 polymorphic loci for the tomtit, which comprises three larger island populations. The black robin displayed a lower number of alleles and expected heterozygosity than the Chatham Island tomtit. We also found that island populations of both species have differentiated from one another, likely due to strong genetic drift acting independently on these populations over a period of isolation. Reciprocal translocations of black robins between islands are recommended to prevent further loss of diversity through drift, and so to improve the probability of species persistence.
... Several studies on NZ birds show evidence for inbreeding depression Hagen et al. 2011;Kennedy et al. 2014;White et al. 2015;Weiser et al. 2016), but results are often marginal or equivocal (Jamieson et al. 2003;Armstrong and Cassey 2007;Grueber et al. 2010;Laws et al. 2010;Laws and Jamieson 2011). A study on the highly inbred black robin gave a particularly interesting result; close inbreeding actually improved fledgling survival for offspring of highly inbred mothers (but not fathers; Weiser et al. 2016). ...
... Several studies on NZ birds show evidence for inbreeding depression Hagen et al. 2011;Kennedy et al. 2014;White et al. 2015;Weiser et al. 2016), but results are often marginal or equivocal (Jamieson et al. 2003;Armstrong and Cassey 2007;Grueber et al. 2010;Laws et al. 2010;Laws and Jamieson 2011). A study on the highly inbred black robin gave a particularly interesting result; close inbreeding actually improved fledgling survival for offspring of highly inbred mothers (but not fathers; Weiser et al. 2016). The authors interpret this result as indicating the benefit of having a 'proven' genotype when highly inbred, as opposed to a novel but equally homozygous genotype-akin to purging. ...
Article
Few areas of conservation biology have grown at quite the same pace as conservation genetics. New Zealand exemplifies this growth with a 50–100-fold increase in publications since a review in 1994. A wide array of techniques in the fields of population genetics, molecular systematics and molecular biology has now become available to conservation biologists to apply to management. Here I review developments categorised broadly into six headings: measuring diversity among individuals; inbreeding; selection and drift; identification of individuals; measuring differentiation (demes, populations, MUs, ESUs, species, hybrids); and other molecular biological approaches. The vast range of available techniques and analyses makes it more important than ever that appropriate tools are chosen for the questions posed, and applied to where need is greatest, if we are to manage our biological diversity successfully in the twenty-first century.
... Recent studies analyzing black robin pedigree data from the intensive management and monitoring period (1982)(1983)(1984)(1985)(1986)(1987)(1988)(1989)(1990)(1991)(1992)(1993)(1994)(1995)(1996)(1997)(1998) have found a high level of inbreeding in the species. The median level of inbreeding, F = 0.34, was found to be much higher than the inbreeding level of offspring produced by full siblings in outbred populations, F = 0.25 (Weiser et al. 2016). The effects of this inbreeding in combination with genetic drift have been shown to lead to the expression of a deleterious, maladaptive trait in the black robin (Massaro et al. 2013a). ...
Article
Full-text available
Dispersal of individuals before their first breeding attempt or between subsequent attempts facilitates spatial and temporal gene flow within and among populations. However, in species on oceanic islands, dispersal is often restricted to a single island, and thus, the risk of inbreeding is particularly high in those small, closed, and isolated populations. One of the mechanisms that may prevent inbreeding within island populations is sex-biased dispersal, which results in close kin of the opposite sex not being in the same area for breeding. In this study, we investigated dispersal patterns, and their costs and benefits, in the Chatham Island black robin, a small passerine confined to two small islands. We found that black robins practice a resource defense mating system as male black robins were more likely to divorce than change territory between breeding seasons. Natal dispersal was female-biased in both the proportion of birds dispersing and the distance dispersed. Bird density in the natal year increased the proportion of birds dispersing in both sexes. Breeding success was reduced for females after natal dispersal. Breeding dispersal was rare and female-biased in proportion only. Regardless of sex, black robins were more likely to disperse after losing a mate, but females dispersed further than males. This study suggests that in closed populations of island species with limited habitat, sex-biased density-dependent dispersal may be a mechanism that minimizes inbreeding. Significance statement Dispersal of individuals facilitates gene flow within and among populations. However, in species on oceanic islands, dispersal is often restricted to movement within a single island. Few studies have investigated dispersal and its costs and benefits in spatially restricted species. Here, we studied the endangered Chatham Island black robin, a songbird confined to two small islands. We found that on an island, where habitat is extremely limited, males are highly territorial and they are more likely to change partners than territories. Bird density in the natal year forces both young males and females to move, but females are more likely to disperse and move further than males. Sex-biased density-dependent dispersal may be a mechanism that minimizes inbreeding. This is particularly important for threatened island endemic species where maintaining high genetic diversity ensures the population’s long-term viability.
... There is still a persistent view (⇠20 respondents) that genetic diversity is not important for all taxa, likely due to ''successes'' such as the Chatham Island black robin (Petroica traversi) and little spotted kiwi (Apteryx owenii), both of which are perceived to have recovered from extreme genetic bottlenecks. In reality, both species are negatively affected by inbreeding depression (Kennedy et al., 2014;Taylor et al., 2017;Weiser et al., 2016). It has been suggested that the benefits of genetics are not fully understood by practitioners (Pierson et al., 2016). ...
Article
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h i g h l i g h t s • Conservation practitioners want to use genetics, but do not routinely do so. • This issue is most acute in control of disease and invasive species. • The main barriers to use of genetics in conservation are funding and expertise. • Practitioners want to work with geneticists, but are unsure how to reach them. • Researchers must facilitate better communication with practitioners. a b s t r a c t Despite its recognised importance for species' persistence, integrating genetics into conservation management has proved problematic, creating a ''conservation genetics gap'', which could widen with the advent of advanced genomic techniques. Bridging this gap requires a clear understanding of the barriers to use of genetics by conservation practitioners, but few (if any) papers on this topic involve direct consultation with practitioners themselves. We surveyed 148 conservation practitioners in New Zealand's Department of Conservation regarding their attitude to, knowledge of, and experiences with genetics for conservation. Although practitioners were largely receptive to using genetics for conservation management , access to expertise and funding remains a barrier to use. Practitioners would like to collaborate with geneticists at universities or other institutes, but do not necessarily know who to talk to or fully understand how genetics might benefit them. We contend these barriers or similar likely exist at an international level, suggest ways they might be overcome, and emphasise the need for clearer communication between geneticists and practitioners.
... These types of studies have revealed that inbreeding occurs frequently in wild populations (reviewed by Kardos et al., 2016), contributing to variation in individual fitness even in populations that are already inbred (e.g. Weiser et al., 2016) or growing (Taylor et al., 2017). Characterizing patterns of inbreeding is therefore an important step in evaluating population viability and understanding the factors that may be limiting population recovery (O'Grady et al., 2006;Frankham, 2010). ...
Article
Full-text available
There are genetic risks associated with small population sizes, including loss of genetic diversity and inbreeding depression. The southern resident killer whale Orcinus orca population is a group of ~80 whales listed as ‘endangered’ under the U.S. Endangered Species Act. Recovery efforts are focused on increasing prey and reducing impacts from environmental disturbance, but the population's small size and insularity suggest that inbreeding depression could also be important. We analyzed genotypes at 68–94 nuclear loci from 105 individuals to refine a population pedigree to evaluate inbreeding and the relationship between multi‐locus heterozygosity and fitness. Our results expand upon an earlier study and shed new light on both inbreeding within this population and the mating patterns of killer whales. We found that only two adult males sired 52% of the sampled progeny born since 1990. Confirming earlier results, we found male reproductive success increased with age. Based on the pedigree, four sampled offspring were the result of inbred mating – two between a parent and offspring, one between paternal half‐siblings, and one between uncle and half‐niece. There is no evidence to date that the survival or fecundity of these individuals is lower than normal. There was some evidence for inbreeding depression in the form of a weakly supported relationship between multi‐locus heterozygosity and annual survival probability, but the power of our data to quantify this effect was low. We found no evidence of inbreeding avoidance in the population, but a late age of breeding success for males may indirectly limit the frequency of parent/offspring mating. The effective number of breeders in the population is currently ~26, and was estimated to have ranged from 12–53 over the past 40 years. The population that produced the oldest (pre‐1970) sampled individuals was estimated to have 24 effective breeders. Overall, our results indicate that inbreeding is likely common in the population, but the fitness effects continue to be uncertain. There are genetic risks associated with small population sizes, including loss of genetic diversity and inbreeding depression. The southern resident killer whale (Orcinus orca) population is a group of ~80 whales listed as ‘endangered’ under the U.S. Endangered Species Act, and due to small population size inbreeding depression is a potential concern. We found that only two adult males sired 52% of the sampled progeny born since 1990. Based on the pedigree, four sampled offspring were the result of inbred mating, however there is no evidence to date that the survival or fecundity of these individuals is lower than normal. Furthermore, we found no evidence of inbreeding avoidance in the population. The effective number of breeders in the population is currently ~26, and was estimated to have ranged from 12–53 over the past 40 years. Overall, our results indicate that inbreeding is likely common in the population, but the fitness effects continue to be uncertain.
... This could simply result from the inbred individuals not being exposed to the cost of raising fledglings (since they produced fewer offspring), although this is rather unlikely as even though helpers of both sexes and dominant males might not have sired offspring, they routinely take care of young on their home territory. A few other studies have reported positive associations between inbreeding and fitness components, which were suggested to be the result of these offspring inheriting a "proven genotype" (i.e., high quality genotype) from a highly inbred parent (Weiser et al. 2016) or by purging and partial dominance of deleterious alleles (Moreno et al. 2015). Despite the limited dispersal in our study population, purging is extremely unlikely as there is no evidence for a recent bottleneck. ...
Article
Full-text available
Extra‐pair paternity (EPP) has been suggested to improve the genetic quality of offspring, but evidence has been equivocal. Benefits of EPP may be only available to specific individuals or under certain conditions. Red‐winged fairy‐wrens have extremely high levels of EPP, suggesting fitness benefits might be large and available to most individuals. Furthermore, extreme philopatry commonly leads to incestuous social pairings, so inbreeding avoidance may be an important selection pressure. Here, we quantified the fitness benefits of EPP under varying conditions and across life‐stages. Extra‐pair offspring (EPO) did not appear to have higher fitness than within‐pair offspring (WPO), neither in poor years nor in the absence of helpers‐at‐the‐nest. However, EPP was beneficial for closely related social pairs, because inbred WPO suffered an overall 75% reduction in fitness. Inbreeding depression was nonlinear and reduced nestling body condition, first year survival and reproductive success. Our comprehensive study indicates that EPP should be favoured for the 17% of females paired incestuously, but cannot explain the widespread infidelity in this species. Furthermore, our finding that fitness benefits of EPP only become apparent for a small part of the population could potentially explain the apparent absence of fitness differences in population wide comparisons of EPO and WPO. This article is protected by copyright. All rights reserved
... Other researchers have found no such effects of inbreeding on direct measures of offspring survival (Kempenaers et al. 1996;Kruuk et al. 2002) or on other traits that could indirectly affect survival, such as the incidence of malformations in larval tiger salamanders (Ambystoma tigrinum tigrinum) (Williams et al. 2008). Finally, somewhat surprisingly, a number of studies have found positive effects of inbreeding on offspring survival (Richardson et al. 2004;Weiser et al. 2016;Bichet et al. 2018). Additionally, it is important to recognize sources of error in calculating effects of inbreeding, which can change across life stages. ...
Article
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Reported effects of inbreeding vary among taxa and may depend on a number of factors, including what trait is measured, temporal variability, parental effects, or life history stage. To understand the effects of inbreeding during early life history stages, we estimated the effects of individual-level heterozygosity on hatching success and first year survival in a Swedish population of sand lizards (Lacerta agilis) over a period of almost a decade, using over 4000 eggs, 400 clutches, and over 3000 juveniles. Heterozygosity had a positive effect on hatching success, in standardized laboratory conditions, but no effect on first year survival. Also, both of these measures of viability varied across the years of the study, demonstrating the importance of temporal heterogeneity in pre and post-hatching conditions. Finally, we identified both paternal and maternal identity effects on hatching success. Thus, we show that selection on heterozygosity was not consistent across developmental life stages, emphasizing the need of considering a number of ontogenic stages, as well as potential parental and environmental effects, when studying the effects of heterozygosity on viability in natural populations.
... Indeed, Soulsbury and Lebigre (2018) A c c e p t e d M a n u s c r i p t 21 negative HFCs among older cohorts, which they attributed to overrepresentation of low heterozygosity-high body mass individuals. Weiser et al. (2016) allude to this idea -that the average 'quality' of inbred individuals improves with age -in a study showing reduced survival of offspring of close relatives but improved survival of offspring of highly inbred mothers. The authors reasoned that inheriting "proven" genotypes could confer fitness advantages. ...
Article
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Inbreeding depression, though challenging to identify in nature, may play an important role in regulating the dynamics of small and isolated populations. Conversely, greater expression of genetic load can enhance opportunities for natural selection. Conditional expression concentrates these opportunities for selection and may lead to failure of detection. This study investigates the possibility for age-dependent expression of inbreeding depression in a critically endangered population of rock iguanas, C. nubila caymanensis. We employ heterozygote-fitness correlations (HFCs) to examine the contributions of individual genetic factors to body size, a fitness-related trait. Non-significant reductions in homozygosity (up to 7%) were detected between neonates and individuals surviving past their first year, which may reflect natural absorption of inbreeding effects by this small, fecund population. The majority of variation in neonate body size was attributed to maternal or environmental effects (i.e. clutch identity and incubation length); however, heterozygosity across 22 microsatellite loci also contributed significantly and positively to model predictions. Conversely, effects of heterozygosity on fitness were not detectable when adults were examined, suggesting that inbreeding depression in body size may be age-dependent in this taxon. Overall, these findings emphasize the importance of taking holistic, cross-generational approaches to genetic monitoring of endangered populations.
... We used Pearson correlation coefficients to identify and exclude highly correlated fixed effects prior to analysis and, in all but one case, dropped correlated fixed effects with coefficients ≥0.60 (Table S2). Location and inter-aviary distance were correlated at 0.79, but both were essential to include as predictors of reproductive success; thus, we retained them in our global GLMM and subsequently evaluated multicollinearity within the GLMM using variance inflation factors (VIF) to ensure that the covariates used in model averaging had VIF < 5 (e.g., Belsley et al., 1980;Weiser et al., 2015). VIFs were calculated using the vif command from the car package (Fox and Weisberg, 2011). ...
Article
Species extinctions are becoming a global crisis, affecting biodiversity and ecosystem services, with island populations being particularly vulnerable. In response, conservation managers are increasingly turning to ex situ conservation breeding programs to establish assurance populations and provide a source for release and re-establishment of wild populations. The 'Alalā (Hawaiian crow, Corvus hawaiiensis) is a critically endangered and territorial island corvid that became extinct in the wild in 2002, following a severe and prolonged population decline during the late 20th century. Surviving individuals of the species were brought into captivity to establish an assurance population to serve as a source for reintroduction, which commenced in 2016. We analyzed the extent to which a range of captive housing conditions impact 'Alalā reproductive success, using 19 years of breeding program data. We found that reproductive success was most strongly affected by the distance between aviaries and their closest neighbors and whether breeding pairs had visual access to other adult conspecifics. Pairs located in aviaries that were more spatially isolated and without visual access to conspecifics were more likely to produce fertile eggs than pairs housed in aviaries that were closer to others or those with visual access to other birds. Our results have direct management implications relevant to the design of conservation breeding centers geared towards the recovery of endangered, territorial bird species. Moreover, since suboptimal housing conditions can increase stress levels in captive birds, our findings are also relevant to improving animal welfare for 'Alalā and other species in conservation breeding programs.
... Inbreeding, the result of mating among close relatives, frequently occurs in small and isolated animal populations, and has a negative influence on most species, ultimately reducing the fitness of offspring and the sustainable survival of the population (Lande, 1988;Kokko & Ots, 2010;Mattey, Strutt & Smiseth, 2013;Weiser et al., 2015). Previous research has suggested that inbreeding could result in a decrease in heterozygosity and increase the expression of deleterious recessive alleles (Fox, 2005). ...
Article
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Inbreeding more likely occurs in small, isolated and endangered populations, and may influence the sustainable survival of a population. As the Amur tiger Panthera tigris altaica population in China experienced a severe decline in the 1990s, the recovering population may be prone to inbreeding and its potential impacts on population health. However, the inbreeding status has not been evaluated and relationships with health remain poorly understood in wild animals. Based on the genetic samples collected from the main Amur tiger habitats in China, this study analyzed the population inbreeding level, major histocompatibility complex polymorphism, parasitic infections and gut microbial structures and functions, and then explored the influence of inbreeding on these traits. Our results indicated that more than 50% of individual relationships were in cousin or half sibs, and 22.73% of individuals had moderate or high inbreeding coefficients. There was a significant positive correlation between the inbreeding level of an individual and the Toxocara cati parasitic load. Gut microbiota community structure and function were also impacted by inbreeding intensity. In conclusion, results indicate that the Amur tiger population in China has reached a moderate level of inbreeding and that there are direct interactions between inbreeding intensity and parasitic load and gut microbiota. This study thus provides an early warning on the Amur tiger population health and should prompt the construction of national and international ecological corridors and/or the re-introduction of new individuals to relieve the evident inbreeding pressure.
... We found that offspring exceeding this threshold were 69% less likely to survive to recruitment than less inbred offspring (F ≤ 0.098). The strong negative effect of inbreeding on 'Alalā offspring survival suggests that genetic purging of recessive deleterious alleles in the population is incomplete and that allelic diversity remains (Weiser et al., 2015), despite the likely occurrence of ancestral inbreeding (Boakes et al., 2007;Sutton et al., 2018). The mean pedigree inbreeding coefficient for the individuals included in our analyses was F = 0.1460, and ranged from 0 to 0.27. ...
Article
Understanding how inbreeding impacts endangered species in conservation breeding programs is essential for their recovery. The 'Alalā (Hawaiian crow, Corvus hawaiiensis) is one of the world's most endangered birds. It went extinct in the wild in 2002, and, as of June 2020, ∼ 90% of the population remains under human care for conservation breeding. Using pedigree inbreeding coefficients (F), we evaluated the effects of inbreeding on 'Alalā offspring survival and reproductive success. In addition, we used regression tree analysis to identify the level of inbreeding, or "inbreeding threshold", that explains a substantial decrease in 'Alalā offspring survival to recruitment. Similar to a previous study of inbreeding depression in 'Alalā, we confirmed that inbreeding has a negative impact on offspring survival but that parental (vs. artificial) egg incubation improves offspring survival to recruitment. By expanding the analysis, we also determined that F does not substantially impact offspring reproductive success, assuming offspring that survive to adulthood breed with distantly related mates. Our novel application of regression tree analysis determined that offspring with inbreeding levels exceeding F = 0.098 were 69% less likely to survive to recruitment than more outbred offspring, providing a specific threshold value for ongoing population management. Our results emphasize the importance of assessing inbreeding depression across all life-history stages, confirm the importance of prioritizing parental over artificial egg incubation in avian conservation breeding programs, and demonstrate the utility of regression tree analysis as a tool for identifying inbreeding thresholds, if present, in any pedigree-managed population. Article impact statement: Regression tree analysis is a useful tool for identifying inbreeding thresholds for genetic management of populations in human care. This article is protected by copyright. All rights reserved.
... Brekke et al., 2010) or, in a few exceptional circumstances, has a positive effect on hatching success (e.g. Weiser et al., 2016). Research on the effects of maternal inbreeding on fertility, egg traits and egg number in wild threatened populations is sorely lacking, despite considerable evidence of these effects in non-threatened species (e.g. ...
Article
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Reproductive failure is ubiquitous. However, research on the mechanisms underpinning reproductive failure is still lacking in most species. This gap in our understanding has particularly strong repercussions for threatened species and it hinders our ability to establish effective interventions to improve survival. In this review, we focus on why eggs fail to hatch – one of the most critical and understudied aspects of bird reproduction. We identify the main drivers of hatching failure in threatened populations of birds and the key mechanisms that cause failure at different stages of development inside the egg. We then discuss the importance of management interventions aimed at reducing hatching failure in species of conservation concern. Our review highlights the need for a better understanding of the mechanistic basis of hatching failure in non‐model bird species and identifies the methodological tools necessary to achieve this.
... The results indicating potential EPP indicate that there may be some inaccuracies within this pedigree, however, since no genetic material still exists from those individuals, we are unable to verify this historical pedigree. This pedigree (extended for a further 10 years) was used to calculate inbreeding coefficients for all individuals on Rangatira Island by adjusting for an estimated EPP rate of < 2% based on rates found in close congeners (Kennedy et al. 2014;Weiser et al. 2016). Assumptions based on EPP rates of closely related species may not account for population processes occurring in the Black Robin, and so may result in inaccurate estimates of inbreeding, fitness, and inbreeding depression depending on the reproductive contributions of males performing EPCs (Reid et al. 2014). ...
Article
Accurate measures of relatedness and inbreeding are important when managing the genetic health of endangered species. However undetected extra-pair parentage, where offspring are the result of copulations outside of the social pair, may result in inaccuracies in relatedness measures if these data are obtained through observing social pairings. Genetic markers present a useful method to detect extra-pair parentage and confirm the accuracy of observed social family groups. With the development of species-specific polymorphic microsatellite loci for the socially monogamous Chatham Island Black Robin (Petroica traversi), it is now possible to investigate extra-pair parentage in this species. Microsatellite genotyping of social family groups allowed us to identify extra-pair paternity in the population on Rangatira Island. The occurrence of extra-pair paternity may have implications for conservation management of this endangered species, as the number of adults contributing to the gene pool is likely different than would be expected from available social pedigree data. While a pedigree is often the best available source of relatedness information for endangered species, it is recommended that where possible, genetic tools should be used to verify pedigree data when informing conservation management decisions.
... Specifically, increases in homozygosity could have exposed deleterious large-effect alleles to selection, thereby removing them from the Stewart Island population and reducing the impact of inbreeding on fitness (Hedrick 1994;Wang et al. 1999;Keller and Waller 2002); although weakly deleterious alleles might still impact individual fitness (i.e., genetic load) (Grossen et al. 2020;Mathur and DeWoody 2021). A study on the Chatham Island black robin, for example, revealed improved fledging success for chicks from highly inbred mothers (Weiser et al. 2016), suggesting Y. Foster et al. | 9 that purging of some of the mutational load may have occurred. We recommend that ongoing conservation management in k ak ap o should focus on detecting individuals exhibiting inbreeding depression and monitoring the effects of mainland ancestry on the population (e.g., F3 hybrids between mainland and Stewart Island). ...
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Events of inbreeding are inevitable in critically endangered species. Reduced population sizes and unique life history traits can increase the severity of inbreeding, leading to declines in fitness and increased risk of extinction. Here, we investigate levels of inbreeding in a critically endangered flightless parrot, the kākāpō (Strigops habroptilus), wherein a highly inbred island population and one individual from the mainland of New Zealand founded the entire extant population. Genotyping-by-sequencing (GBS), and a genotype calling approach using a chromosome-level genome assembly, identified a filtered set of 12,241 single nucleotide polymorphisms (SNPs) among 161 kākāpō, which together encompass the total genetic potential of the extant population. Multiple molecular-based estimates of inbreeding were compared, including genome-wide estimates of heterozygosity (FH), the diagonal elements of a genomic-relatedness matrix (FGRM), and runs of homozygosity (RoH, FRoH). Additionally, we compared levels of inbreeding in chicks from a recent breeding season to examine if inbreeding is associated with offspring survival. The density of SNPs generated with GBS was sufficient to identify chromosomes that were largely homozygous with RoH distributed in similar patterns to other inbred species. Measures of inbreeding were largely correlated and differed significantly between descendants of the two founding populations. However, neither inbreeding nor ancestry were found to be associated with reduced survivorship in chicks, owing to unexpected mortality in chicks exhibiting low levels of inbreeding. Our study highlights important considerations for estimating inbreeding in critically endangered species, such as the impacts of small population sizes and admixture between diverse lineages.
... However, in wild populations, the effective size is usually much smaller than the actual number of breeding adults (Frankham 1995;Vucetich et al. 1997;Palstra and Ruzzante 2008). Furthermore, the effective size of many endangered populations has progressively declined down to values on the order of tens, as in the cases the Chatham Island black robin Petroica traversi (Ardern and Lambert 1997;Weiser et al. 2016) or the Fennoscandian arctic fox Vulpes lagopus (Angerbjörn et al. 2013;Norén et al. 2016), and many others. In some of these cases, population growth is limited by non-genetic factors, as habitat or prey limitations (Adams et al. 2011;Hedrick et al. 2014). ...
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Genetic rescue is increasingly considered a promising and underused conservation strategy to reduce inbreeding depression and restore genetic diversity in endangered populations, but the empirical evidence supporting its application is limited to a few generations. Here we discuss on the light of theory the role of inbreeding depression arising from partially recessive deleterious mutations and of genetic purging as main determinants of the medium to long-term success of rescue programs. This role depends on two main predictions: (1) The inbreeding load hidden in populations with a long stable demography increases with the effective population size; and (2) After a population shrinks, purging tends to remove its (partially) recessive deleterious alleles, a process that is slower but more efficient for large populations than for small ones. We also carry out computer simulations to investigate the impact of genetic purging on the medium to long term success of genetic rescue programs. For some scenarios, it is found that hybrid vigor followed by purging will lead to sustained successful rescue. However, there may be specific situations where the recipient population is so small that it cannot purge the inbreeding load introduced by migrants, which would lead to increased fitness inbreeding depression and extinction risk in the medium to long term. In such cases, the risk is expected to be higher if migrants came from a large non-purged population with high inbreeding load, particularly after the accumulation of the stochastic effects ascribed to repeated occasional migration events. Therefore, under the specific deleterious recessive mutation model considered, we conclude that additional caution should be taken in rescue programs. Unless the endangered population harbors some distinctive genetic singularity whose conservation is a main concern, restoration by continuous stable gene flow should be considered, whenever feasible, as it reduces the extinction risk compared to repeated occasional migration and can also allow recolonization events.
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A pivotal debate on biodiversity conservation is whether the scarce budgets must be invested in critically endangered taxa or in those with higher chances to survive due to larger population sizes. Addressing the fate of extremely bottlenecked taxa is an ideal way to test this idea, but empirical cases are surprisingly limited. The reintroduction of the extinct‐in‐the‐wild Alagoas curassow (Pauxi mitu) by Brazilian scientists in September 2019 added to the two other known cases of survival to bottlenecks of only two or three individuals. We exploit the reasons why this species has survived, and we report how investments to rescue the Alagoas curassow resulted in the protection of many other taxa, suggesting that in the face of the dramatic number of extinctions expected for the Anthropocene, integration must prevail over a choice. Highlights • Alagoas curassow was the first extinct‐in‐the‐wild species to be reintroduced in South America. This species had one of the most severe bottlenecks ever recorded for a vertebrate, and all remaining individuals descend from three founders. After careful ex‐situ and genetic management, the captive population had heterozygosity recovering, allowing some individuals to be released in their natural habitat after 40 years from the last record.
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Genetic rescue is increasingly considered a promising and underused conservation strategy to reduce inbreeding depression and restore genetic diversity in endangered populations, but the empirical evidence supporting its application is limited to a few generations. Here we discuss on the light of theory the role of inbreeding depression arising from partially recessive deleterious mutations and of genetic purging as main determinants of the medium to long-term success of rescue programs. This role depends on two main predictions: (1) The inbreeding load hidden in populations with a long stable demography increases with the effective population size; and (2) After a population shrinks, purging tends to remove its (partially) recessive deleterious alleles, a process that is slower but more efficient for large populations than for small ones. We also carry out computer simulations to investigate the impact of genetic purging on the medium to long term success of genetic rescue programs. For some scenarios, it is found that hybrid vigor followed by purging will lead to sustained successful rescue. However, there may be specific situations where the recipient population is so small that it cannot purge the inbreeding load introduced by migrants, which would lead to increased fitness inbreeding depression and extinction risk in the medium to long term. In such cases, the risk is expected to be higher if migrants came from a large non-purged population with high inbreeding load, particularly after the accumulation of the stochastic effects ascribed to repeated occasional migration events. Therefore, under the specific deleterious recessive mutation model considered, we conclude that additional caution should be taken in rescue programs. Unless the endangered population harbors some distinctive genetic singularity whose conservation is a main concern, restoration by continuous stable gene flow should be considered, whenever feasible, as it reduces the extinction risk compared to repeated occasional migration and can also allow recolonization events.
Article
Inbreeding depression, the reduction of fitness caused by inbreeding, is a nearly universal phenomenon that depends on past mutation, selection, and genetic drift. Recent estimates suggest that its impact on individual fitness is even greater than previously thought. Genomic information is contributing to its detection and can enlighten important aspects of its genetic architecture. In natural populations, purging and genetic rescue mitigate fitness decline during inbreeding periods, and might be critical to population survival, thus, both mechanisms should be considered when assessing extinction risks. However, deliberate purging and genetic rescue involve considerable risk in the short and medium term, so that neither appears to be a panacea against high inbreeding depression.
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Description Fit linear and generalized linear mixed-effects models. The models and their components are represented using S4 classes and methods. The core computational algorithms are implemented using the 'Eigen' C++ library for numerical linear algebra and 'RcppEigen' ``glue''.
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Inbreeding (mating between relatives) can dramatically reduce the fitness of offspring by causing parts of the genome to be identical by descent. Thus, measuring individual inbreeding is crucial for ecology, evolution and conservation biology. We used computer simulations to test whether the realized proportion of the genome that is identical by descent (IBD G) is predicted better by the pedigree inbreeding coefficient (F P) or by genomic (marker-based) measures of inbreeding. Genomic estimators of IBD G included the increase in individual homozygosity relative to mean Hardy–Weinberg expected homozygosity (F H), and two measures (F ROH and F E) that use mapped genetic markers to estimate IBD G. IBD G was more strongly correlated with F H , F E and F ROH than with F P across a broad range of simulated scenarios when thousands of SNPs were used. For example, IBD G was more strongly correlated with F ROH , F H and F E (estimated with ⩾ 10 000 SNPs) than with F P (estimated with 20 generations of complete pedigree) in populations with a recent reduction in the effective populations size (from N e = 500 to N e = 75). F ROH , F H and F E generally explained 490% of the variance in IBD G (among individuals) when 35 K or more SNPs were used. F P explained o80% of the variation in IBD G on average in all simulated scenarios, even when pedigrees included 20 generations. Our results demonstrate that IBD G can be more precisely estimated with large numbers of genetic markers than with pedigrees. We encourage researchers to adopt genomic marker-based measures of IBD G as thousands of loci can now be genotyped in any species.
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Extra-pair copulation without apparent direct benefits is an evolutionary puzzle that requires indirect fitness benefits to females to explain its ubiquity in socially monogamous mating systems. Using wild scarlet rosefinches (Carpodacus erythrinus), we tested if genetic benefits in the form of global (microsatellite) heterozygote advantage, adaptive genes (major histocompatibility complex), or complementary genes (using both markers) were responsible for female extra-pair mate choice, while considering that the benefits of mate choice may be conditional on female genotype. We found no evidence for assortative or relatedness-based mating (complementary genes), but higher MHC diversity, microsatellite heterozygosity, and condition were significantly related to male extra-pair paternity (EPP) success. In contrast, female probability of having extra-pair offspring decreased with increasing heterozygosity. Interestingly, extra-pair and within-pair males had higher heterozygosity than their female mates and extra-pair males had higher MHC supertype diversity. The only genetic difference between extra-pair and within-pair offspring was lower variance in MHC allelic diversity within extra-pair offspring, providing limited support for indirect genetic fitness benefits for the markers tested. Offspring had both higher neutral heterozygosity and number of MHC supertypes than adults, as well as significant identity disequilibrium, potentially suggesting that mates are chosen to increase offspring diversity in the period of the present study. Overall, our results point to an EPP heterozygote advantage for males, especially when involving less heterozygous females, and suggest that heterozygosity effects on reproduction may differ between the sexes.
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Conservation management often focuses on counteracting the adverse effects of human activities on threatened populations. However, conservation measures may unintentionally relax selection by allowing the 'survival of the not-so-fit', increasing the risk of fixation of maladaptive traits. Here, we report such a case in the critically-endangered Chatham Island black robin (Petroica traversi) which, in 1980, was reduced to a single breeding pair. Following this bottleneck, some females were observed to lay eggs on the rims of their nests. Rim eggs left in place always failed to hatch. To expedite population recovery, rim eggs were repositioned inside nests, yielding viable hatchlings. Repositioning resulted in rapid growth of the black robin population, but by 1989 over 50% of all females were laying rim eggs. We used an exceptional, species-wide pedigree to consider both recessive and dominant models of inheritance over all plausible founder genotype combinations at a biallelic and possibly sex-linked locus. The pattern of rim laying is best fitted as an autosomal dominant Mendelian trait. Using a phenotype permutation test we could also reject the null hypothesis of non-heritability for this trait in favour of our best-fitting model of heritability. Data collected after intervention ceased shows that the frequency of rim laying has strongly declined, and that this trait is maladaptive. This episode yields an important lesson for conservation biology: fixation of maladaptive traits could render small threatened populations completely dependent on humans for reproduction, irreversibly compromising the long term viability of populations humanity seeks to conserve.
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Although evidence of inbreeding depression in wild populations is well established, the impact of genetic purging in the wild remains controversial. The contrasting effects of inbreeding depression, fixation of deleterious alleles by genetic drift, and the purging of deleterious alleles via natural selection mean that predicting fitness outcomes in populations subjected to prolonged bottlenecks is not straightforward. We report results from a long-term pedigree study of arguably the world's most inbred wild species of bird: the Chatham Island black robin Petroica traversi, in which conditions were ideal for purging to occur. Contrary to expectations, black robins showed a strong, negative relationship between inbreeding and juvenile survival, yielding lethal equivalents (2B) of 6.85. We also determined that the negative relationship between inbreeding and survival did not appear to be mediated by levels of ancestral inbreeding and may be attributed in part to unpurged lethal recessives. Although the black robin demographic history provided ideal conditions for genetic purging, our results show no clear evidence of purging in the major life-history trait of juvenile survival. Our results also show no evidence of fixation of deleterious alleles in juvenile survival, but do confirm that continued high levels of contemporary inbreeding in a historically inbred population could lead to additional severe inbreeding depression.
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Matings between close relatives often reduce the fitness of offspring, probably because homozygosity leads to the expression of recessive deleterious alleles1, 2, 3, 4, 5. Studies of several animals have shown that reproductive success is lower when genetic similarity between parents is high4, 5, 6, 7, and that survival and other measures of fitness increase with individual levels of genetic diversity8, 9, 10, 11. These studies indicate that natural selection may favour the avoidance of matings with genetically similar individuals. But constraints on social mate choice, such as a lack of alternatives, can lead to pairing with genetically similar mates. In such cases, it has been suggested that females may seek extra-pair copulations with less related males4, but the evidence is weak or lacking4, 5. Here we report a strong positive relationship between the genetic similarity of social pair members and the occurrence of extra-pair paternity and maternity ('quasi-parasitism') in three species of shorebirds. We propose that extra-pair parentage may represent adaptive behavioural strategies to avoid the negative effects of pairing with a genetically similar mate.
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It has been proposed that inbreeding contributes to the decline and eventual extinction of small and isolated populations,. There is ample evidence of fitness reduction due to inbreeding (inbreeding depression) in captivity and from a few experimental, and observational field studies,, but no field studies on natural populations have been conducted to test the proposed effect on extinction. It has been argued that in natural populations the impact of inbreeding depression on population survival will be insignificant in comparison to that of demographic and environmental stochasticity,. We have now studied the effect of inbreeding on local extinction in a large metapopulation of the Glanville fritillary butterfly (Melitaea cinxia). We found that extinction risk increased significantly with decreasing heterozygosity, an indication of inbreeding, even after accounting for the effects of the relevant ecological factors. Larval survival, adult longevity and egg-hatching rate were found to be adversely affected by inbreeding and appear to be the fitness components underlying the relationship between inbreeding and extinction. To our knowledge, this is the first demonstration of an effect of inbreeding on the extinction of natural populations. Our results are particularly relevant to the increasing number of species with small local populations due to habitat loss and fragmentation.
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Inbreeding is assumed to have negative effects on fitness, including the reduced ability to withstand immune challenges. We examined the immunological consequences of inbreeding in decorated crickets, Gryllodes sigillatus, by comparing lytic activity, phenoloxidase (PO) activity, and encapsulation ability of crickets from eight inbred lines with that of crickets from the outbred founder population. Surprisingly, crickets from inbred lines had a greater encapsulation ability compared with crickets from the outbred population. We suggest that because inbred crickets have reduced reproductive effort, they may, therefore, have the option of devoting more resources to this form of immunity than outbred individuals. We also found that both inbred and outbred females had higher immunity than males in PO activity and implant darkness. This result supports the hypothesis that females should devote more effort to somatic maintenance and immunity than males. PO activity and implant darkness were heritable in both males and females, but lytic activity was only heritable in females. Males and females differed in the heritability of, and genetic correlations among, immune traits, suggesting that differences in selective pressures on males and females may have resulted in a sexual conflict over optimal immune trait values.
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Inbreeding depression - the reduced survival and fertility of offspring of related individuals - occurs in wild animal and plant populations as well as in humans, indicating that genetic variation in fitness traits exists in natural populations. Inbreeding depression is important in the evolution of outcrossing mating systems and, because intercrossing inbred strains improves yield (heterosis), which is important in crop breeding, the genetic basis of these effects has been debated since the early twentieth century. Classical genetic studies and modern molecular evolutionary approaches now suggest that inbreeding depression and heterosis are predominantly caused by the presence of recessive deleterious mutations in populations.
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Sex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood. Several explanations based on asymmetrical inheritance patterns (sex chromosomes or mitochondrial DNA) have been proposed, but these ideas have rarely been tested experimentally. Alternatively, sexual dimorphism in lifespan could result from sex-specific selection, caused by fundamental differences in how males and females optimize their fitness by allocating resources into current and future reproduction. Here we used sex-specific responses to inbreeding to study the genetic architecture of lifespan and mortality rates in Callosobruchus maculatus, a seed beetle that shows sexual dimorphism in lifespan. Two independent assays revealed opposing sex-specific responses to inbreeding. The combined data set showed that inbred males live longer than outbred males, while females show the opposite pattern. Both sexes suffered reduced fitness measured as lifetime reproductive success as a result of inbreeding. No model based on asymmetrical inheritance can explain increased male lifespan in response to inbreeding. Our results are however compatible with models based on sex-specific selection on reproductive strategies. We therefore suggest that sex-specific differences in lifespan in this species primarily result from sexually divergent selection.
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R package for Data Analysis using multilevel/hierarchical model
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Tools for performing model selection and model averaging. Automated model selection through subsetting the maximum model, with optional constraints for model inclusion. Model parameter and prediction averaging based on model weights derived from information criteria (AICc and alike) or custom model weighting schemes. [Please do not request the full text - it is an R package. The up-to-date manual is available from CRAN].
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Natal dispersal is a key life-history component that may be influenced by the fitness consequences of inbreeding. We studied natal dispersal and inbreeding within a large population of cooperatively breeding, endangered Red-cockaded Woodpeckers (Picoides borealis). We assessed the costs of close inbreeding, the spatial distribution of related males and its relationship to dispersal distance of females, and the change in dispersal behavior of females in the presence of closely related males. Close inbreeding resulted in a significant loss of fitness, through two separate effects: closely related pairs (kinship coefficient ≥ 0.125) exhibited lowered hatching rates and lowered survival and recruitment of fledglings relative to unrelated pairs. Despite a highly predictable spatial clustering of closely related males near the female's natal territory, natal dispersal distance of females was not sufficient to avoid these males as mates. Females changed dispersal behavior in the presence of closely related males on the natal territory: female fledglings were significantly more likely to disperse from natal territories if there were closely related males breeding there in the following year. Females did not change dispersal behavior in the presence of related males that were not on the natal territory. We suggest that dispersal behavior is a trade-off between benefits of short-distance dispersal, e.g., an advantage in competing for scarce breeding vacancies, and the substantial cost of close inbreeding.
Article
Accumulation of deleterious mutations has important consequences for the evolution of mating systems and the persistence of small populations. It is well established that consanguineous mating can purge a part of the mutation load and that lethal mutations can also be purged in small populations. However, the efficiency of purging in natural populations, due to either consanguineous mating or to reduced population size, has been questioned. Consequences of consanguineous mating systems and small population size are often equated under “inbreeding” because both increase homozygosity, and selection is though to be more efficient against homozygous deleterious alleles. I show that two processes of purging that I call “purging by drift” and “purging by nonrandom mating” have to be distinguished. Conditions under which the two ways of purging are effective are derived. Nonrandom mating can purge deleterious mutations regardless of their dominance level, whereas only highly recessive mutations can be purged by drift. Both types of purging are limited by population size, and sharp thresholds separate domains where purging is either effective or not. The limitations derived here on the efficiency of purging are compatible with some experimental studies. Implications of these results for conservation and evolution of mating systems are discussed.
Article
Inbreeding depression is thought to be a major factor affecting the evolution of mating systems and dispersal. While there is ample evidence for inbreeding depression in captivity, it has rarely been documented in natural populations. In this study, I examine data from a long-term demographic study of an insular population of song sparrows (Melospiza melodia) and present evidence for inbreeding depression. Forty-four percent of all matings on Mandarte Island, British Columbia, were among known relatives. Offspring of a full-sib mating (f = 0.25) experienced a reduction in annual survival rate of 17.5% on average. Over their lifetime, females with f = 0.25 produced 48% fewer young that reached independence from parental care. In contrast, male lifetime reproductive success was not affected by inbreeding. Reduced female lifetime reproductive success was mostly due to reduced hatching rates of the eggs of inbred females. Relatedness among the parents did not affect their reproductive success. Using data on survival from egg stage to breeding age, I estimated the average song sparrow egg on Mandarte Island to carry a minimum of 5.38 lethal equivalents (the number of deleterious genes whose cumulative effect is equivalent to one lethal); 2.88 of these lethal equivalents were expressed from egg stage to independence of parental care. This estimate is higher than most estimates reported for laboratory populations and lower than those reported for zoo populations. Hence, the costs of inbreeding in this population were substantial and slightly above those expected from laboratory studies. Variability in estimates of lethal equivalents among years showed that costs of inbreeding were not constant across years.
Article
During the long-term population study of the Great Tit, all nestlings were ringed and most parents were identified. This allows the construction of family-trees. In an island population of about 50 pairs we found a common ancestor in 19% of the clutches where both parents were identified and in 47% of the clutches where the geneaologies were completely known up to the grandparents of the pair. The hatching of eggs is reduced by 7.5% for every 10% increase of F. The effect of inbreeding is smaller at the moment of fledging. The recruitment to the next generation at breeding age is not lower from related pairs than from other pairs with the same clutch size in the same year. There is a separate effect on the hatching rate if the female is inbred. However the recruitment from clutches where either the male or the female is inbred is twice as high as expected. This can be explained because a few individuals have produced many offspring. The offspring have a high chance of mating with a relative, but the adverse effects of inbreeding are offset by higher recruitment. There is no evidence that inbreeding is avoided. Neither is it clear that inbreeding avoidance would be selectively advantageous.
Book
Limitations of linear regression applied on ecological data. - Things are not always linear additive modelling. - Dealing with hetergeneity. - Mixed modelling for nested data. - Violation of independence - temporal data. - Violation of independence spatial data. - Generalised linear modelling and generalised additive modelling. - Generalised estimation equations. - GLMM and GAMM. - Estimating trends for Antarctic birds in relation to climate change. - Large-scale impacts of land-use change in a Scottish farming catchment. - Negative binomial GAM and GAMM to analyse amphibian road killings. - Additive mixed modelling applied on deep-sea plagic bioluminescent organisms. - Additive mixed modelling applied on phyoplankton time series data. - Mixed modelling applied on American Fouldbrood affecting honey bees larvae. - Three-way nested data for age determination techniques applied to small cetaceans. - GLMM applied on the spatial distribution of koalas in a fragmented landscape. - GEE and GLMM applied on binomial Badger activity data.
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Introduction and Historical PerspectiveTechnical Background Experimental ExperienceSummary Interpretation, and Examples of Diagnosing Actual Data for CollinearityAppendix 3A: The Condition Number and InvertibilityAppendix 3B: Parameterization and ScalingAppendix 3C: The Weakness of Correlation Measures in Providing Diagnostic InformationAppendix 3D: The Harm Caused by Collinearity
Article
Molecular estimates of inbreeding may be made using genetic markers such as microsatellites, however the interpretation of resulting heterozygosity-fitness correlations (HFCs) with respect to inbreeding depression is not straightforward. We investigated the relationship between pedigree-determined inbreeding coefficients (f) and HFCs in a closely monitored, reintroduced population of Stewart Island robins (Petroica australis rakiura) on Ulva Island, New Zealand. Using a full sibling design, we focused on differences in juvenile survival associated specifically with individual sibling variation in standardized multilocus heterozygosity (SH) when expected f was identical. We found that within broods, siblings with higher SH at microsatellite loci experienced a higher probability of juvenile survival. This effect, however, was detected primarily within broods that experienced inbreeding or when inbreeding had occurred in their pedigree histories (i.e., at the parents' level). Thus we show, for the first time in a wild population, that the strength of an HFC is partially dependent on the presence of inbreeding events in the recent pedigree history. Our results illustrate the importance of realized effects of inbreeding on genetic variation and fitness and the value of full-sibling designs for the study of HFCs in the context of small, inbred populations.
Article
In three adjacent troops of olive baboons (Papio anubis), all males emigrated from their natal troop. There is evidence that the costs of inbreeding depression may exceed those of transferring to another troop. Migrations which were unlikely to be due to the avoidance of inbreeding were made by males with above average reproductive activity into troops with more oestrous females than the prior troop. During inter-troop encounters, immigrant (‘transferred’) males acted in ways that reduced the contact of females of their own troop with outsiders and lowered the probability of newcomers joining the troop. In contrast, ‘natal’ males showed interest in members of the other troop. Male dominance was strongly related to age, and in transferred males reproductive activity was related to dominance. In natal males dominance increased with age but reproductive activity decreased. Instead of engaging in aggressive competition for access to oestrous females, natalmales mated surreptitiously. Females showed a preference for transferred males over natal males, and for males who could not have been their father over males who could have been.
Article
Individual-based estimates of the degree of inbreeding or parental relatedness from pedigrees provide a critical starting point for studies of inbreeding depression, but in practice wild pedigrees are difficult to obtain. Because inbreeding increases the proportion of genomewide loci that are identical by descent, inbreeding variation within populations has the potential to generate observable correlations between heterozygosity measured using molecular markers and a variety of fitness related traits. Termed heterozygosity-fitness correlations (HFCs), these correlations have been observed in a wide variety of taxa. The difficulty of obtaining wild pedigree data, however, means that empirical investigations of how pedigree inbreeding influences HFCs are rare. Here, we assess evidence for inbreeding depression in three life-history traits (hatching and fledging success and juvenile survival) in an isolated population of Stewart Island robins using both pedigree- and molecular-derived measures of relatedness. We found results from the two measures were highly correlated and supported evidence for significant but weak inbreeding depression. However, standardized effect sizes for inbreeding depression based on the pedigree-based kin coefficients (k) were greater and had smaller standard errors than those based on molecular genetic measures of relatedness (RI), particularly for hatching and fledging success. Nevertheless, the results presented here support the use of molecular-based measures of relatedness in bottlenecked populations when information regarding inbreeding depression is desired but pedigree data on relatedness are unavailable.
Article
Natal dispersal is a key life-history component that may be influenced by the fitness consequences of inbreeding. We studied natal dispersal and inbreeding within a large population of cooperatively breeding, endangered Red-cockaded Woodpeckers (Picoides borealis). We assessed the costs of close inbreeding, the spatial distribution of related males and its relationship to dispersal distance of females, and the change in dispersal behavior of females in the presence of closely related males. Close inbreeding resulted in a significant loss of fitness, through two separate effects: closely related pairs (kinship coefficient ≥ 0.125) exhibited lowered hatching rates and lowered survival and recruitment of fledglings relative to unrelated pairs. Despite a highly predictable spatial clustering of closely related males near the female's natal territory, natal dispersal distance of females was not sufficient to avoid these males as mates. Females changed dispersal behavior in the presence of closely related males on the natal territory: female fledglings were significantly more likely to disperse from natal territories if there were closely related males breeding there in the following year. Females did not change dispersal behavior in the presence of related males that were not on the natal territory. We suggest that dispersal behavior is a trade-off between benefits of short-distance dispersal, e.g., an advantage in competing for scarce breeding vacancies, and the substantial cost of close inbreeding.
Article
Inbreeding is commonly associated with a lowering of viability and birth weights—a phenomenon known as inbreeding depression. A severe inbreeding depression was encountered in a captive breeding program for Speke's gazelle. Unfortunately, the solution of simply avoiding inbreeding could not be implemented because the entire herd was descended from one import male and three import females. Because of this founder effect, it was impossible to avoid inbreeding. However, laboratory experiments with fruit flies and basic evolutionary theory indicate that animals can rapidly adapt to inbreeding by the selective elimination of the genes responsible for inbreeding depression. These experimental and theoretical results were translated into a breeding program for the Speke's gazelle. The first goal of the breeding program is a demographic goal: increase the total population size as rapidly as possible to the carrying capacity. The other goals all deal with genetic attributes of either parents or offspring: Both parents and offspring should be inbred, and both parents and offspring should have genes from as many different founding ancestors as possible. In this paper, we document that this breeding program does eliminate the inbreeding depression very rapidly, and moreover that the genetic goals of the program aid this elimination exactly as theory predicts. Furthermore, our analysis clearly shows that the gazelles suffered from an inbreeding depression rather than an outcrossing depression. We conclude that inbreeding depressions can be rapidly and effectively reduced by an appropriate breeding program, and hence an inbreeding depression does not constitute an insurmountable barrier to the long-term maintenance of a species in which inbreeding cannot be avoided.
Article
The importance of inbreeding avoidance for the fitness of individuals is currently undergoing reevahation. Especially when the frequency of inbreeding is low, it may be difficult to accumulate sufficient information. In a long-term study of the Mexican jay (Aphelocoma ultamarina) in Arizona, we found inbreeding, as determined by pedigree, to be rare even though this species exhibits strong natal philopatry and commonly lives in social groups of close relatives. Brood sizes of inbred pairs were significantly lower than those of outbred pairs, suggesting hatching failure; but there was no difference in die probability that one or more young would fledge from a nest. Survival of inbred nestlings to die next year was significantly lower than that of outbred nestlings.
Article
Fitness is expected to decrease with inbreeding in proportion to the amount of deleterious genetic variation present in a population. The effect of inbreeding on survivorship is usually modeled as a negative exponential relationship, and this model has been widely used to estimate the amount of deleterious genetic varia-tion in populations. Linear regression has traditionally been used to estimate the parameters of the model, including the number of lethal equivalents. This article describes an alternative method for estimating parameters and their confidence limits: the maximum likelihood approach. The accuracy of regression and maxi-mum likelihood estimates of the number of lethal equivalents is compared through simulation. The maximum likelihood approach is found to be both median unbi-ased and capable of estimating confidence limits with nearly the stated degree of accuracy, while the linear regression approach is found to be median biased. The significance of this on previous estimates of inbreeding depression is discussed.
Article
In 1980 the entire black robin species Petroica traversi comprised only five birds, and the current population of ≊ 200 individuals is known to be derived from a single breeding pair. We show here that levels of minisatellite DNA variation in the black robin are among the lowest reported for any avian species in the wild. Surprisingly, similarly bottlenecked control populations of a closely related species (P. australis australis) exhibit significantly higher levels of genetic variation. This suggests that the black robin's persistence in a single small population for the last 100 years, rather than the recent bottleneck itself, accounts for the low genetic variation observed. Despite apparent genetic impoverishment, survival and reproductive performance indicate that the black robin is viable under existing conditions. This example illustrates that significant levels of genetic variation are not a necessary prerequisite for endangered species' survival.
Article
Summary1. Linear regression models are an important statistical tool in evolutionary and ecological studies. Unfortunately, these models often yield some uninterpretable estimates and hypothesis tests, especially when models contain interactions or polynomial terms. Furthermore, the standard errors for treatment groups, although often of interest for including in a publication, are not directly available in a standard linear model.2. Centring and standardization of input variables are simple means to improve the interpretability of regression coefficients. Further, refitting the model with a slightly modified model structure allows extracting the appropriate standard errors for treatment groups directly from the model.3. Centring will make main effects biologically interpretable even when involved in interactions and thus avoids the potential misinterpretation of main effects. This also applies to the estimation of linear effects in the presence of polynomials. Categorical input variables can also be centred and this sometimes assists interpretation.4. Standardization (z-transformation) of input variables results in the estimation of standardized slopes or standardized partial regression coefficients. Standardized slopes are comparable in magnitude within models as well as between studies. They have some advantages over partial correlation coefficients and are often the more interesting standardized effect size.5. The thoughtful removal of intercepts or main effects allows extracting treatment means or treatment slopes and their appropriate standard errors directly from a linear model. This provides a simple alternative to the more complicated calculation of standard errors from contrasts and main effects.6. The simple methods presented here put the focus on parameter estimation (point estimates as well as confidence intervals) rather than on significance thresholds. They allow fitting complex, but meaningful models that can be concisely presented and interpreted. The presented methods can also be applied to generalised linear models (GLM) and linear mixed models.
Article
High rates of extra-pair paternity (EPP) can be relatively common in passerines whereas low rates or absence of EPP are often associated with taxa that are long-lived and exhibit obligatory paternal care. We examined EPP in an under-represented category: passerine species with relatively long life spans (or low annual mortality rates). Specifically, we studied EPP in New Zealand saddlebacks Philesturnus carunculatus and robins Petroica australis, two species with unusually low annual mortality rates (6.5–11% and 10–20% respectively). No EPP (0%) was detected in saddlebacks (39 pairs, 202 offspring) and only one case of EPP (1.9%) was detected in robins (54 pairs, 198 offspring). Genetic monogamy in these passerine species supports the hypothesis that low annual mortality rates play an important role in explaining variation in rates of EPP across species.
Article
Model averaging, specifically information theoretic approaches based on Akaike’s information criterion (IT-AIC approaches), has had a major influence on statistical practices in the field of ecology and evolution. However, a neglected issue is that in common with most other model fitting approaches, IT-AIC methods are sensitive to the presence of missing observations. The commonest way of handling missing data is the complete-case analysis (the complete deletion from the dataset of cases containing any missing values). It is well-known that this results in reduced estimation precision (or reduced statistical power), biased parameter estimates; however, the implications for model selection have not been explored. Here we employ an example from behavioural ecology to illustrate how missing data can affect the conclusions drawn from model selection or based on hypothesis testing. We show how missing observations can be recovered to give accurate estimates for IT-related indices (e.g. AIC and Akaike weight) as well as parameters (and their standard errors) by utilizing ‘multiple imputation’. We use this paper to illustrate key concepts from missing data theory and as a basis for discussing available methods for handling missing data. The example is intended to serve as a practically oriented case study for behavioural ecologists deciding on how to handle missing data in their own datasets and also as a first attempt to consider the problems of conducting model selection and averaging in the presence of missing observations. KeywordsData augmentation–Data deletion–Estimation bias–The rate of missing information–Expectation maximization–QAIC–EPP–MCMC–House sparrows
Article
Numerous studies have reported associations between heterozygosity in microsatellite markers and fitness-related traits (heterozygosity-fitness correlations, HFCs). However, it has often been questioned whether HFCs reflect general inbreeding depression, because a small panel of microsatellite markers does not reflect very well an individual's inbreeding coefficient (F) as calculated from a pedigree. Here, we challenge this prevailing view. Because of chance events during Mendelian segregation, an individual's realized proportion of the genome that is identical by descent (IBD) may substantially deviate from the pedigree-based expectation (i.e. F). This Mendelian noise may result in a weak correlation between F and multi-locus heterozygosity, but this does not imply that multi-locus heterozygosity is a bad estimator of realized IBD. We examined correlations between 11 fitness-related traits measured in up to 1192 captive zebra finches and three measures of inbreeding: (i) heterozygosity across 11 microsatellite markers, (ii) heterozygosity across 1359 single-nucleotide polymorphism (SNP) markers and (iii) F, based on a 5th-generation pedigree. All 11 phenotypic traits showed positive relationships with measures of heterozygosity, especially traits that are most closely related to fitness. Remarkably, the small panel of microsatellite markers produced equally strong HFCs as the large panel of SNP markers. Both marker-based approaches produced stronger correlations with phenotypes than the pedigree-based F, and this did not seem to result from the shortness of our pedigree. We argue that a small panel of microsatellites with high allelic richness may better reflect an individual's realized IBD than previously appreciated, especially in species like the zebra finch, where much of the genome is inherited in large blocks that rarely experience cross-over during meiosis.
Article
Inbreeding depression, which refers to reduced fitness among offspring of related parents, has traditionally been studied using pedigrees. In practice, pedigree information is difficult to obtain, potentially unreliable, and rarely assessed for inbreeding arising from common ancestors who lived more than a few generations ago. Recently, there has been excitement about using SNP data to estimate inbreeding (F) arising from distant common ancestors in apparently "outbred" populations. Statistical power to detect inbreeding depression using SNP data depends on the actual variation in inbreeding in a population, the accuracy of detecting that with marker data, the effect size, and the sample size. No one has yet investigated what variation in F is expected in SNP data as a function of population size, and it is unclear which estimate of F is optimal for detecting inbreeding depression. In the present study, we use theory, simulated genetic data, and real genetic data to find the optimal estimate of F, to quantify the likely variation in F in populations of various sizes, and to estimate the power to detect inbreeding depression. We find that F estimated from runs of homozygosity (Froh), which reflects shared ancestry of genetic haplotypes, retains variation in even large populations (e.g., SD=0.5% when Ne=10,000) and is likely to be the most powerful method of detecting inbreeding effects from among several alternative estimates of F. However, large samples (e.g., 12,000-65,000) will be required to detect inbreeding depression for likely effect sizes, and so studies using Froh to date have probably been underpowered.
Article
Fragmentation of animal and plant populations typically leads to genetic erosion and increased probability of extirpation. Although these effects can usually be reversed by re-establishing gene flow between population fragments, managers sometimes fail to do so due to fears of outbreeding depression (OD). Rapid development of OD is due primarily to adaptive differentiation from selection or fixation of chromosomal variants. Fixed chromosomal variants can be detected empirically. We used an extended form of the breeders' equation to predict the probability of OD due to adaptive differentiation between recently isolated population fragments as a function of intensity of selection, genetic diversity, effective population sizes, and generations of isolation. Empirical data indicated that populations in similar environments had not developed OD even after thousands of generations of isolation. To predict the probability of OD, we developed a decision tree that was based on the four variables from the breeders' equation, taxonomic status, and gene flow within the last 500 years. The predicted probability of OD in crosses between two populations is elevated when the populations have at least one of the following characteristics: are distinct species, have fixed chromosomal differences, exchanged no genes in the last 500 years, or inhabit different environments. Conversely, the predicted probability of OD in crosses between two populations of the same species is low for populations with the same karyotype, isolated for <500 years, and that occupy similar environments. In the former case, we recommend crossing be avoided or tried on a limited, experimental basis. In the latter case, crossing can be carried out with low probability of OD. We used crosses with known results to test the decision tree and found that it correctly identified cases where OD occurred. Current concerns about OD in recently fragmented populations are almost certainly excessive.
Article
Information theoretic approaches and model averaging are increasing in popularity, but this approach can be difficult to apply to the realistic, complex models that typify many ecological and evolutionary analyses. This is especially true for those researchers without a formal background in information theory. Here, we highlight a number of practical obstacles to model averaging complex models. Although not meant to be an exhaustive review, we identify several important issues with tentative solutions where they exist (e.g. dealing with collinearity amongst predictors; how to compute model-averaged parameters) and highlight areas for future research where solutions are not clear (e.g. when to use random intercepts or slopes; which information criteria to use when random factors are involved). We also provide a worked example of a mixed model analysis of inbreeding depression in a wild population. By providing an overview of these issues, we hope that this approach will become more accessible to those investigating any process where multiple variables impact an evolutionary or ecological response.
Article
New Zealand ecologists and wildlife managers have assumed traditionally that threatened insular endemic bird species are less susceptible to the predicted genetic consequences of declines and inbreeding. Conservation has relied on treating deterministic extinction pressures to trigger population recoveries, with few measures taken to minimise stochastic genetic threats to long-term viability. This study tested that assumption empirically by exam-ining extinction vulnerability in two small, critically threatened Chatham Island black robin populations protected from external threats on habitat-restricted islands but not man-aged purposefully for genetic health. Analysis of the factors eliminating the species’s original island populations indicated loss through habitat change and mammalian predation within perhaps no more than two to three decades of human contact. Loss was undoubtedly hastened by intrinsic extinction-proneness (low reproductive output, forest-interior preference, sensitivity to habitat quality, intolerance of open spaces), greater in black robins than in other Petroica species in New Zealand and Australia. Low productivity in ancestral survivors prevented spontaneous recovery after translocation to better habitat, requiring intensively assisted breeding to raise population sizes quickly. Strong growth in response to management did not suggest a moribund species but post-management growth rates were significantly slower. Analysis of demographic data from 1980-81 to 2001-02 showed breeding effort to be comparable in all populations but breeding failures of varying severity at different life-history stages affected natural recovery in each. The worst affected suf-fered from briefer adult life-spans and more severe failure late in the breeding cycle. Generally colder sub-canopy air temperatures suggested adverse environmental pressure on this population. Extant populations are highly inbred and severely depleted genetically fol-lowing successive bottlenecks (prolonged historically) and recovery from a single-pair event between 1979-80 and 1982-83. At current small sizes, accumulating levels of relat-edness are anomalously high. Contrary to perceptions that black robin recovery indicates normal fitness, viability was shown to be threatened by inbreeding depression expressed cumulatively in the breeding cycle as low juvenile production and survival, thus aggravating a principal vulnerability. Declines did not result during the study period and effects were limited to reproductive fitness costs in black robin fathers only. There was no evi-dence of harmful effects on survival probability or from maternal inbreeding but an emerging kinship effect on yearling production is possible. The restricted costs in such highly inbred populations (relative to less inbred congeners) suggest historical purging of genetic load. Work is needed to clarify this and the extent to which inbreeding could reduce re-sponses to new extinction pressures. Recent population declines may elevate levels of in-breeding further. Genetic management is strongly recommended, including habitat expan-sion to maximise population sizes and prevent further cross-breeding with a sympatric congener. Management and monitoring recommendations apply valuable lessons derived from a critique of past practices. In summary, findings give qualified support to the hy-pothesis of reduced susceptibility to inbreeding depression in threatened insular endemic birds. Findings do not support the assumption implicit in black robin management historically and in New Zealand wildlife management practice generally that stochastic genetic threats are unimportant risks to viability.
Article
BLDSC reference no.: D19917/77. Thesis (doctoral)--University of Sussex, 1977.
Article
Captive-breeding programs have been widely used in the conservation of imperiled species, but the effects of inbreeding, frequently expressed in traits related to fitness, are nearly unavoidable in small populations with few founders. Following its planned extirpation in the wild, the endangered red wolf (Canis rufus) was preserved in captivity with just 14 founders. In this study, we evaluated the captive red wolf population for relationships between inbreeding and reproductive performance and fitness. Over 30 years of managed breeding, the level of inbreeding in the captive population has increased, and litter size has declined. Inbreeding levels were lower in sire and dam wolves that reproduced than in those that did not reproduce. However, there was no difference in the inbreeding level of actual litters and predicted litters. Litter size was negatively affected by offspring and paternal levels of inbreeding, but the effect of inbreeding on offspring survival was restricted to a positive influence. There was no apparent relationship between inbreeding and method of rearing offspring. The observable effects of inbreeding in the captive red wolf population currently do not appear to be a limiting factor in the conservation of the red wolf population. Additional studies exploring the extent of the effects of inbreeding will be required as inbreeding levels increase in the captive population.
Article
Inbreeding depression has been a topic of interest in recent years from a number of perspectives, particularly in the captive breeding of endangered species. Generally, the goal of captive breeding is to avoid the detrimental effects of inbreeding depression and to retain genetic variation for future adaptation. However, an important component of another suggested approach to captive breeding is to purge rapidly the population of its genetic load so that its long-term fitness is not compromised. I have examined the effectiveness of purging the genetic load by documenting both the reduction in inbreeding depression and the increase of the probability of extinction when there is continuous full-sib mating. When the genetic load is the result of lethals, the inbreeding depression is quickly purged without a high probability of extinction, except when the total genetic load is high. On the other hand, if the load is due to detrimentals of relatively small effect, the genetic load becomes fixed, the mean fitness is reduced, and the probability of extinction may be greatly increased. In other words, the success of such a programme to purge genetic load without an increase in the probability of extinction is highly dependent upon the genetic basis of inbreeding depression, information that is not readily available for most species.