Inbreeding depression and the maintenance of genetic load in Melitaea cinxia metapopulations (original) (raw)
Related papers
Evolution, 2000
We investigated the effects of inbreeding on various fitness components and their genetic load in laboratory metapopulations of the butterfly Bicyclus anynana. Six metapopulations each consisted of four subpopulations with breeding population sizes of N ϭ 6 or N ϭ 12 and migration rate of m ϭ 0 or m ϭ 0.33. Metapopulations were maintained for seven generations during which coancestries and pedigrees were established. Individual inbreeding coefficients at the F 7 were calculated and ranged between 0.01 and 0.51. Even though considerable purging had occurred during inbreeding, the genetic load remained higher than that of many outbreeding species: approximately two lethal equivalents were detected for egg sterility, one for zygote survival, one for juvenile survival, and one for longevity. Severe inbreeding depression occurred after seven generations of inbreeding, which jeopardized the metapopulation survival. This finding suggests that the purging of genetic load by intentional inbreeding cannot be recommended for the genetic conservation of species with a high number of lethal equivalents.
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 .
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.
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.
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.
Biodiversity and Conservation, 2000
We investigated the genetic population structure of two rare myrmecophilous lycaenid butterflies, Maculinea nausithous and M. teleius, which often live sympatrically and have similar biology. In Europe, both species occur in highly fragmented populations and are vulnerable to local extinction. The proportion of variable allozyme loci, average heterozygosity and genetic differentiation among populations was higher in M. nausithous than in sympatrically living M. teleius populations. We hypothesise that the differences in heterozygosity are mainly due to the known higher efficiency of typical host ant nests in rearing M. nausithous pupae compared to M. teleius pupae. This implies a larger probability of larval survival in M. nausithous, which buffers populations against environmental and demographic stochasticity. In contrast, the lower carrying capacity of ant nests in rearing M. teleius pupae requires higher nest-densities and makes M. teleius populations more prone to losing genetic variation through drift if this condition is not fulfilled. The single investigated Russian population of M. teleius showed much higher levels of heterozygosity than any of the Polish populations, suggesting a more viable and still intact metapopulation structure.
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.