Inbreeding Depression and Genetic Load in Laboratory Metapopulations of the Butterfly Bicyclus Anynana (original) (raw)
Related papers
2000
The effect of small population size and gene flow on the rate of inbreeding and loss in fitness in Bicyclus anynana populations was quantified by means of a pedigree analysis. Laboratory metapopulations each consisted of four subpopulations with breeding size of N = 6 or N = 12 and migration rate of m = 0 or m = 0.33. Pedigrees were established by individually marking about 35,000 butterflies. The increase in inbreeding coefficients (F-coefficients) over time was compared to that of simulated populations with similar N and m. In the seventh generation, the level of inbreeding in larger subpopulations did not deviate significantly from the expected values, but smaller subpopulations were less inbred than expected. Individuals in the small populations still showed considerable inbreeding depression, indicating that only a small proportion of the recessive deleterious alleles had been purged by selection. Two opposing processes potentially affected the rate of inbreeding and fitness: (1) Inbreeding depression increased the variance in family size and reduced the effective population size. This will accelerate the rate of inbreeding and is expected to selectively purge deleterious recessive alleles. (2) Variance in reproductive success of families was reduced because individuals which had a large number of siblings in the population were more likely to mate with a full-sib than individuals with a smaller number of siblings. Subsequent inbreeding depression reduced the number of viable offspring produced by these full-sib matings. As a consequence, natural selection purged only some of the deleterious alleles from the butterfly populations during seven generations with inbreeding. These findings emphasise the potential problems of using only small numbers of breeding individuals (N ≤ 10) in captive populations for conservation purposes.
Inbreeding and extinction in a butterfly metapopulation
Nature, 1998
It has been proposed that inbreeding contributes to the decline and eventual extinction of small and isolated populations 1,2 . There is ample evidence of fitness reduction due to inbreeding (inbreeding depression) in captivity 3-7 and from a few experimental 8,9 and observational field studies 10,11 , 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 12,13 . We have now studied the effect of inbreeding on local extinction in a large metapopulation 14 of the Glanville fritillary butterfly (Melitaea cinxia) 15 . We found that extinction risk increased significantly with decreasing heterozygosity, an indication of inbreeding 6 , 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 16 .
Proceedings of The Royal Society B: Biological Sciences, 2005
Inbreeding depression is most pronounced for traits closely associated with fitness. The traditional explanation is that natural selection eliminates deleterious mutations with additive or dominant effects more effectively than recessive mutations, leading to directional dominance for traits subject to strong directional selection. Here we report the unexpected finding that, in the butterfly Bicyclus anynana, male sterility contributes disproportionately to inbreeding depression for fitness (complete sterility in about half the sons from brother-sister matings), while female fertility is insensitive to inbreeding. The contrast between the sexes for functionally equivalent traits is inconsistent with standard selection arguments, and suggests that trait-specific developmental properties and cryptic selection play crucial roles in shaping genetic architecture. There is evidence that spermatogenesis is less developmentally stable than oogenesis, though the unusually high male fertility load in B. anynana additionally suggests the operation of complex selection maintaining male sterility recessives. Analysis of the precise causes of inbreeding depression will be needed to generate a model that reliably explains variation in directional dominance and reconciles the gap between observed and expected genetic loads carried by populations. This challenging evolutionary puzzle should stimulate work on the occurrence and causes of sex differences in fertility load.
Inbreeding depression and the maintenance of genetic load in Melitaea cinxia metapopulations
2001
The effects of inbreeding on fitness and the maintenance of genetic load in metapopulations of the endangered Glanville fritillary butterfly (Melitaea cinxia) were examined in four laboratory experiments. In Finland M. cinxia occurs as a large metapopulation consisting of small local populations with fast turnover, whereas in southern France the species has a more continuous population structure. In the experiments, we compared the performance of crosses between full sibs, crosses between members of different families within populations, and crosses between individuals from different populations. These experiments were replicated using insects from two different regions, Finland and southern France, between which the frequency of natural inbreeding should differ substantially because of differing population structure. In Finnish butterflies, the rate of successful mating was lower among insects derived from small than from large natural populations, probably reflecting the effect of past inbreeding history. Mating between full sibs lowered egg hatching rate in all experiments. This reduction of egg hatching rate was more severe among French butterflies with a more continuous population structure than among Finnish butterflies with small naturally fragmented populations and with a history of repeated rounds of inbreeding in the past. This result suggests that recurrent inbreeding has led to partial purging of deleterious recessives from the Finnish metapopulation. Nonetheless, substantial genetic load still remains in this metapopulation, and we discuss possible reasons why this should be the case.
1999
Polymorphic enzyme and minisatellite loci were used to estimate the degree of inbreeding in experimentally bottlenecked populations of the butterfly, Bicyclus anynana (Satyridae), three generations after founding events of 2, 6, 20, or 300 individuals, each bottleneck size being replicated at least four times. Heterozygosity fell more than expected, though not significantly so, but this traditional measure of the degree of inbreeding did not make full use of the information from genetic markers. It proved more informative to estimate directly the probability distribution of a measure of inbreeding, 2 , the variance in the number of descendants left per gene. In all bottlenecked lines, 2 was significantly larger than in control lines (300 founders). We demonstrate that this excess inbreeding was brought about both by an increase in the variance of reproductive success of individuals, but also by another process. We argue that in bottlenecked lines linkage disequilibrium generated by the small number of haplotypes passing through the bottleneck resulted in hitchhiking of particular marker alleles with those haplotypes favored by selection. In control lines, linkage disequilibrium was minimal. Our result, indicating more inbreeding than expected from demographic parameters, contrasts with the findings of previous (Drosophila) experiments in which the decline in observed heterozygosity was slower than expected and attributed to associative overdominance. The different outcomes may both be explained as a consequence of linkage disequilibrium under different regimes of inbreeding. The likelihood-based method to estimate inbreeding should be of wide applicability. It was, for example, able to resolve small differences in 2 among replicate lines within bottleneck-size treatments, which could be related to the observed variation in reproductive viability.
Effects of bottlenecks on quantitative genetic variation in the butterfly Bicyclus anynana
Genetics Research, 2001
The effects of a single population bottleneck of differing severity on heritability and additive genetic variance was investigated experimentally using a butterfly. An outbred laboratory stock was used to found replicate lines with one pair, three pairs and 10 pairs of adults, as well as control lines with approximately 75 effective pairs. Heritability and additive genetic variance of eight wing pattern characters and wing size were estimated using parent-offspring covariances in the base population and in all daughter lines. Individual morphological characters and principal components of the nine characters showed a consistent pattern of treatment effects in which average heritability and additive genetic variance was lower in one pair and three pair lines than in 10 pair and control lines. Observed losses in heritability and additive genetic variance were significantly greater than predicted by the neutral additive model when calculated with coefficients of inbreeding estimated from demographic parameters alone. However, use of molecular markers revealed substantially more inbreeding, generated by increased variance in family size and background selection. Conservative interpretation of a statistical analysis incorporating this previously undetected inbreeding led to the conclusion that the response to inbreeding of the morphological traits studied showed no significant departure from the neutral additive model. This result is consistent with the evidence for minimal directional dominance for these traits. In contrast, egg hatching rate in the same experimental lines showed strong inbreeding depression, increased phenotypic variance and rapid response to selection, highly indicative of an increase in additive genetic variance due to dominance variance conversion.
High genetic load in an old isolated butterfly population
We investigated inbreeding depression and genetic load in a small (Ne ∼ 100) population of the Glanville fritillary butterfly (Melitaea cinxia), which has been completely isolated on a small island [Pikku Tytärsaari (PT)] in the Baltic Sea for at least 75 y. As a reference, we studied conspecific populations from the well-studied metapopulation in the Åland Islands (ÅL), 400 km away. A large population in Saaremaa, Estonia, was used as a reference for estimating genetic diversity and Ne.We investigated 58 traits related to behavior, development, morphology, reproductive performance, and metabolism. The PT population exhibited high genetic load (L = 1 − WPT/WÅL) in a range of fitness-related traits including adult weight (L = 0.12), flight metabolic rate (L = 0.53), egg viability (L = 0.37), and lifetime production of eggs in an outdoor population cage (L = 0.70). These results imply extensive fixation of deleterious recessive mutations, supported by greatly reduced diversity in microsatellite markers and immediate recovery (heterosis) of egg viability and flight metabolic rate in crosses with other populations. There was no significant inbreeding depression in most traits due to one generation of full-sib mating. Resting metabolic rate was significantly elevated in PT males, which may be related to their short lifespan (L = 0.25). The demographic history and the effective size of the PT population place it in the part of the parameter space in which models predict mutation accumulation. This population exemplifies the increasingly common situation in fragmented landscapes, in which small and completely isolated populations are vulnerable to extinction due to high genetic load.