Can inbreeding increase population fitness

Herfindal et al. Because calf sex and weight category carcass or live weight may affect body mass, we included these two variables and their interactions in all candidate models. In the models, we further tested the effects of f and MLH of calves, mothers and fathers, mother and father age, mother parity, litter size, and the population size and adult sex ratio in the calving year. As climate variables, we used spring and summer temperatures in the year of calving. Year and cow identity was added as random factors.

In addition, we included cow f and MLH , her age and parity, and the population size at her year of birth. We also tested the interactions of f or MLH with age and parity. As climate variables, we added spring and summer temperature from the birth year of the cow.

The shape of the relationship between cow age and asLRS was unknown and we therefore first ran a generalized additive mixed model gamm, Wood between asLRS and age with cow birth year as a random factor to explore linearity. We therefore used a generalized linear mixed model with poisson error structure and a log link function, and cow birth year as random factor.

The ln-transformed cow age was included as covariate in addition to cow f and MLH , and population size at the cows' year of birth. As for the twinning rate, we included the interactions between f or MLH and cow age, and used spring and summer temperatures at the cows' year of birth as climate variables. Significant deviations from Hardy—Weinberg equilibrium were only found in two cohorts for one locus RT6 and BM among the 22 applied loci.

After Bonferroni correction, significant linkage disequilibrium was only found between nine pairs of loci distributed among 6 years, as compared to the pairs of loci tested each of the 25 years.

The combined nonexclusion probability of an unrelated candidate parent was 0. Expected heterozygosity ranged from 0. Allelic richness ranged from 2. Among the individuals in the pedigree, the average level of inbreeding f across years was 0. The general trend through time was an increasing degree of inbreeding and a slight decrease in heterozygosity Fig. The reduction in level of inbreeding in , and and after coincides with periods when most immigration took place four immigrants —, eight immigrants —, and five immigrants in — Shortly after each of these reductions, the level of inbreeding rapidly increased again.

Individual heterozygosity MLH ranged from 0. From heterozygosity across loci, g 2 was estimated to be 0. For both f and MLH, there was a correlation between offspring and parents f Calf vs. The best model explaining variation in birth date included calf f , population size, and whether the mother was primiparous or not Table 1 A. Moreover, the sum of AICc weights of candidate models including f was higher 0.

AICc-based ranking of models explaining variation in individual birth date. A The best models considering the following individual and population parameters as explanatory variables: inbreeding coefficient f and heterozygosity MLH of the calf, its mother and its father, age of the mother and father Age , number of siblings 1,0 , mother parity Primiparous , population size N , and adult sex ratio ASR. The highest ranked model in bold had an AICc-value of For details regarding the global model and selection procedure, see Methods.

Relationship between fitness-related traits and the inbreeding coefficient f for moose on Vega. B Winter live body mass of male calves. C Twinning rate for calving females. Calf body mass was best explained by calf f , mother MLH , mother age, mother parity Table 2 A , as well as calf sex and weight category always retained in the models, see Methods.

AICc-based ranking of candidate models explaining variation in calf body mass. A The best models based on individual and population parameters as explanatory variables. In addition, sex Sex , and weight category calf carcass mass or calf winter mass and their interaction were always retained in the models.

B The best models when adding climate variables to the most parsimonious model in A. See Table 1 for variables explanation. The twinning rate was best explained by the f -value of the cow, whether she was primiparous or multiparous, and population size in the year of calving.

Alternative models had little support Table 3 A. Moreover, the sum of AICc weights from models including f 0. Adding climate variables from the cows' year of birth did not improve the fit Table 3 B. AICc-based ranking of models explaining the variation in cow twinning rates. A The best models based on individual parameters and population size in the year of birth N Birth and year of calving N.

B The best models after including climate variables in the most parsimonious model in A. The best model had an AICc-value of The sum of AICc-w for candidate models including f 0.

As we focus on inbreeding effects, we used the second best model to explore the effects of climate, but allowed model selection to exclude f from the candidate models. Consequently, there was no support for inbreeding effects on the asLRS. AICc-based ranking of candidate models explaining cow age-specific lifetime reproductive success asLRS. A The best models including individual parameters and population size at birth year N.

B The highest ranked models after including climate variables to the most parsimonious model in A. The best model in bold had an AICc-value of This suggests strong genetic drift, as was expected from the few founders and subsequently low population size.

However, albeit a low genetic variation, genetic parentage assignment was significant in most individuals. This high agreement between genetic and socially determined maternities provides credibility to previous ecological investigations at Vega e. In accordance with the low population size, the level of inbreeding calculated from the pedigree f was high.

The level of inbreeding was reduced following immigration but shortly after increased again Fig. The variance in f was also high, as can be expected when inbred populations contain immigrants and their descendants Reid et al. The relatedness structure subsequent to immigration also explains the correlation in f between offspring and each parental sex Reid et al. A low variation in f is often reported from wild populations Grueber et al. With a limited number of loci, random segregation in each locus may also have an effect Slate et al.

We detected a negative correlation between f and MLH, indicating a sufficient mean and variance in f compared to the number of loci. The correlation in homozygosity across loci suggests a genome-wide effect Szulkin et al. We found negative effects of inbreeding on three fitness-related traits Tables 3 and Fig. Inbreeding may operate on different life history stages Szulkin et al. Surprisingly, we did not find any inbreeding effects on female age-specific lifetime reproductive success, but this was probably because of few individuals with data on asLRS and hence low statistical power.

By comparison, significant effects of inbreeding have been found on the lifetime reproductive success in other ungulates Slate et al. Indeed, inbreeding depression seems to be stronger in traits that are closely related to fitness De Rose and Roff ; Wright et al. The later date of birth for inbred calves may have two explanations: 1 that conception occurs later in the rut for inbred than for more outbred calves and 2 that inbreeding involves a longer gestation period.

Variation in conception date can occur as a result of varying cow condition at the onset of rut Garel et al. Given the strong effect of juvenile body mass on adult body mass Solberg et al. Therefore, as the date of birth was unaffected by the level of inbreeding in mothers and fathers, we find it unlikely that inbreeding effects on cow conditions or mate choice caused the later birth dates of inbred calves.

More likely, variation in gestation length can explain some variation in birth date, for example, if inbred fetuses have slower growth. Schwarts et al. Hence, there seems to be some flexibility in the length of the gestation period of ungulates.

One benefit of early birth is that calves have longer access to high-quality forage, which can have profound effects on body growth and fitness in large herbivores e. Moreover, as cold springs involve better forage and faster moose growth Herfindal et al.

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You have authorized LearnCasting of your reading list in Scitable. Do you want to LearnCast this session? This article has been posted to your Facebook page via Scitable LearnCast. Change LearnCast Settings. In theory, purging of deleterious alleles will reduce the costs of inbreeding over time and fitness may be recovered, or even enhanced [ 34 ]. While some studies suggest the relationship between population fitness and inbreeding can be influenced by purging [ 35 , 36 ], several reviews indicate the effectiveness of purging is highly variable [ 37 , 38 ].

The investigation of the impact of purging requires inbreeding to be followed across multiple generations. The map shows that the primary research in natural populations is limited, with most studies only assessing one generation of inbreeding.

Similar limitations on studies of outbreeding responses have also been noted [ 15 ]. In addition, information on factors that can influence the effectiveness of purging, such as the rate of inbreeding classified here as population history; [ 36 ] , are poorly reported in natural populations.

Measuring the costs of inbreeding across multiple generations, and the potential for purging, is not straightforward, particularly in natural populations, but it may be critical to elucidating the long-term consequences of inbreeding in natural populations.

To be maximally informative for conservation, studies need to assess the effects of inbreeding using scenarios that mimic those found in nature. However, this aim typically conflicts with obtaining robust and repeatable results that control for and disentangle potentially confounding variables.

Several studies indicate that the costs of inbreeding increase, or may only become apparent under more stressful conditions [ 21 , 39 ]. Thus, while measures under controlled conditions may increase accuracy, it does not necessarily reflect the costs of inbreeding that would occur under natural conditions, which may be much greater.

The map does, however, show that while numerous studies continue to assess inbreeding under controlled environments, the number of studies assessing the costs under natural conditions has increased e. Substantial variation in the costs of inbreeding has been documented e. This map shows that individual studies rarely assessed multiple species or multiple populations within a species in an attempt to document variation and fewer attempted to test potential causes.

Variation in inbreeding responses could be related to species- or population- specific attributes, or other study specific effects, which need to be considered when interpreting the phenotypic effects of inbreeding reported. Information on the potential sources of heterogeneity we were interested in was reported sporadically. Population level effects such as size, levels of genetic diversity and demographic history were relatively poorly reported compared with potential experimental effects such as the environmental context traits were measured under.

It is also likely the map underestimates the number of studies where relevant additional information on species and population level effects is available, as it may be reported in separate articles or it may be available through consultation with authors. Nonetheless, the lack of reporting of potential sources of variation is likely to represent a pervasive problem within the inbreeding literature and is a common criticism of primary research synthesised in other reviews [ 15 , 42 ].

Understanding the influence of potential sources of variation on the effects of inbreeding can inform decision-making in conservation and enable the prediction of high-risk situations where intervention may be required. In general, the consequences of inbreeding are based on outcrossing diploids species [ 4 ]. Thus, the first step in assessing risk is an understanding of species traits. However, the map shows there is substantial variation in reporting of many traits, while sufficient data on the mode of reproduction appears to exist; information on the ploidy of study species appears insufficient to enable review.

Among populations within species potentially useful proxies for identifying high-risk situations include levels of genetic diversity within populations e. Genetic diversity is typically measured at neutral loci, which do not impact on fitness, and as a result measures of neutral and quantitative variation do not always correlate [ 45 ]. Thus, the underlying cause of the correlation between levels of neutral genetic diversity measures such as heterozygosity and fitness is not well resolved [ 43 ].

The map shows that while not extensive, sufficient studies exist to support syntheses to further elucidate the extent to which measures of neutral genetic diversity can reflect genetic load and hence the costs of inbreeding. From a practical standpoint, estimates of population size may be more easily obtained and frequently form part of monitoring and risk assessment.

Hence determining the relationship between census size and inbreeding is likely to be useful for managers. Although the effective population size, the equivalent number of individuals contributing to the next generation is more closely related to inbreeding risk, it is difficult to determine and previous studies have shown census population size correlates with both effective population size and genetic diversity [ 43 , 46 ]. The relationship between inbreeding depression and census size is not straightforward as shown in a recent meta-analysis in plants [ 20 ].

Thus, broader reviews are required to provide insights into this relationship and refine predictions. The systematic map shows sufficient studies exist for meta-analysis to further elucidate the potential for census size to predict inbreeding depression but see Possible systematic review topics below. The systematic map highlights several areas in the primary research that are less well explored in natural populations. The long-term, multigenerational consequences of inbreeding, especially the potential for the restoration of fitness via purging of genetic load.

The extent and causes of variation in inbreeding responses across populations of the same species, and particularly in response to differences in population size or levels of within-population neutral genetic diversity. The systematic map highlights several subtopics that contain suitable primary research for synthesis into a systematic review.

This systematic map revealed two distinct lines of investigation into inbreeding responses; the consequences of inbreeding resulting from consanguineous matings within populations and the impacts due to isolation and drift.

The latter is likely encompassed by a recent systematic review of the consequences of outbreeding [ 15 ] and further review at this time is unlikely to yield additional information. Specific questions could include:. Plants were clearly the focus of the primary research with studies in the map and hence a review could provide relatively robust conclusions, although the high proportion of studies employing self-fertilisation may limit the relevance of these conclusions to other taxonomic groups.

A subset of these data, relating to population size has already been meta-analysed but see the following point. The primary research for invertebrates and vertebrates is sparser but could still be informative, particularly in vertebrates where studies often assess inbreeding under natural conditions.

How does population size influence the costs of inbreeding in natural populations? Information on the relationship between inbreeding costs and population size has the potential to inform conservation strategy as a proxy for risks assessment. This area has recently been meta-analysed for plants [ 20 ]. This review was not systematic but future meta-analyses would need to ascertain potential overlap.

The primary research will support a similar review on animals. How do levels of neutral genetic variation within populations affect the costs of inbreeding? How does the environmental context influence phenotypic responses to inbreeding? The search strategy and the repeatability of the inclusion criteria were relatively robust to missing relevant studies based on sensitivity analyses of the searches and kappa analyses of inclusion criteria.

In these cases, it is possible that neither of the two published articles may be covered by the search strategy. In addition, although we employed a broad definition of inbreeding designed to capture primary literature investigating both within- and among-population inbreeding [ 47 ], it is possible that some studies assessing among-population inbreeding were published as outcrossing studies, and so may not have been covered by our searches.

There are also limitations associated with interpreting the results of queries in the database, due to the independent coding of attributes for each study. This occurs because each study may measure multiple variables or cross types, but not all the potential combinations of these may have been assessed.

For instance, a study may report survival under controlled conditions but growth rate under both natural and controlled conditions. In the database the study will be recorded as measuring the traits survival and growth rate and that traits were measured under natural and controlled conditions. Thus, the record would imply that both traits were measured under natural conditions even though survival was only measure in controlled conditions. This was limited, to some extent, by the separation of articles into studies where multiple species or experimental designs were employed but could not be overcome without loss of detail or further dissection of records into individual observations.

Searches and screening procedures were carried out according to the original systematic review protocol, including kappa analyses.

Articles were categorised according to the experimental design, sources of heterogeneity and the quality of the study. The map provides a research tool for managers interested in the potential consequences of inbreeding and can be used to gather data for a range of subtopics. The information provided will enable users to identify relevant publications and assess the amount of information and, importantly, the quality of this information for a given topic.

The map also highlights the potential for secondary syntheses to generate information that could be incorporated into conservation planning. The map highlights several areas where information is limited or lacking and suggests future primary research should aim to assess the longer term multi-generational impacts of inbreeding, across multiple populations and under natural conditions.

In addition, studies that simultaneously investigate within-population and among-population inbreeding are required to strengthen and refine our understanding of situations where inbreeding depression may not be detected due to the fixation of genetic load. Finally, the potential for meta-analysis to be used to investigate the factors influencing variation in the phenotypic consequences of inbreeding appears limited, with the map showing a lack of reporting about potential sources of heterogeneity.

This is particularly important from a conservation perspective where these patterns can lead to the identification of useful proxies for predicting the risks posed by inbreeding depression. Frankham R. Inbreeding in the wild really does matter.

Inbreeding effects in wild populations. Trends Ecol Evol. Article Google Scholar. Most species are not driven to extinction before genetic factors impact them. Introduction to Conservation Genetics. Cambridge: Cambridge University Press; Book Google Scholar. Charlesworth D, Willis JH. The genetics of inbreeding depression. Nat Rev Genet. Charlesworth B, Charlesworth D. The genetic basis of inbreeding depression. Genet Res. Reevaluating and broadening the definition of genetic rescue.

Conserv Biol. Hedrick P, Fredrickson R. Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv Genet. Genetic restoration of the Florida panther. Novel genes continue to enhance population growth in adders Vipera berus. Biol Conserv. Conservation Biology: restoration of an inbred adder population. Genetic rescue persists beyond first-generation outbreeding in small populations of a rare plant. Edmands S. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management.

Mol Ecol. Lynch M. The genetic interpretation of inbreeding depression and outbreeding depression. A systematic review of phenotypic responses to between-population outbreeding. Environ Evid. Predicting the probability of outbreeding depression. Inbreeding depression in conservation biology. Annu Rev Ecol Syst. Crnokrak P, Roff DA. Inbreeding depression in the wild. Heredity Edinb. Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Meta-analysis on the association of population size and life history with inbreeding depression in plants.

Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Grant MJ, Booth A. A typology of reviews: an analysis of 14 review types and associated methodologies.

Heal Inf Libr J. Google Scholar. Ferris R. In spite of the negative consequences on any conscious increase of inbreeding for the long term viability of a captive population managed under an EEP, if rigorously conducted upon previous and scientifically based knowledge of that population genetic, demographic, behavioural,… , it might represent a better management option than culling.

We thank Daniel Benzal for helping in tissue preparation. Two anonymous reviewers improve an earlier version of the manuscript. Conceived and designed the experiments: EM. Performed the experiments: EM. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract Captive breeding of endangered species often aims at preserving genetic diversity and to avoid the harmful effects of inbreeding.

This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Data Availability: All relevant data are within the paper and its Supporting Information files. Introduction Captive breeding is a valuable tool for the preservation of endangered species, and in some instances it may turn out to be the only possible way to avoid total extinction.

DNA sampling and genetic analyses To study genetic effects at the population level after the change in management, we compared heterozygosity before and after the change. Download: PPT. Discussion The deleterious effect of inbreeding is of major concern in conservation biology. Supporting Information. S1 File. S2 File.

Author Contributions Conceived and designed the experiments: EM. References 1. John Murray, London. Heredity — Zoo Biol — View Article Google Scholar 6. Hedrick PW Purging inbreeding depression and the probability of extinction: full-sib mating. Zschoekke S, Baur B Inbreeding, outbreeding, infant growth, and size dimorphism in captive Indian Rhinoceros Rhinoceros unicornis. Can J Zool — View Article Google Scholar 8. Mol Ecol — Fox CW, Reed DH Inbreeding depression increases with environmental stress: an experimental study and meta-analysis.

Evolution — Charlesworth D, Charlesworth B Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst — View Article Google Scholar Roff DA Inbreeding depression: tests of the overdominance and partial dominance hypotheses. Nat Rev Genet — Nature — Hedrick PW Lethals in finite populations.

Drift versus nonrandom mating. Crnokrak P, Barret SC Perspective: purging the genetic load: a review of the experimental evidence. Science — Genet Res — Conserv Biol — Ecology and Evolution — Wang J Effect of population structures and selection strategies on the purging of inbreeding depression due to deleterious mutations.

Genetic Res Camb — Robert A Captive breeding genetic and reintroduction success. Biol Conserv — TREE — J Zool Lond — Proc R Soc Lond B — Cassinello J Inbreeding depression on reproductive performance and survival in captive gazelles of great conservation value.

Mamm Biol — Animal Conservation — Fredrickson R, Hedrick P Body size in endangered Mexican wolves: Effects of inbreeding and cross-lineage matings. Joron M, Brakefield PM Captivity masks inbreeding effects on male mating success in butterflies.