Effects of bottlenecks on quantitative genetic variation in the butterfly Bicyclus anynana (original) (raw)
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Biological Journal of the Linnean Society, 2006
The consequences of population bottlenecks for morphological differentiation were investigated experimentally in the Afrotropical butterfly Bicyclus anynana (Satyrinae). A genetically variable laboratory population was used to establish daughter populations differing in the severity of the founding bottleneck (two, six, 20 and c. 300 individuals), with four to six replicate lines per treatment. Nine quantitative traits of the hind wing were measured (wing area and eight wing pattern characters) in the founders, F 1 , F 2 and F 3 generations. A tenth character, egg weight, was measured in all lines in F 3. The validity of the neutral additive model was tested by regressing the observed phenotypic variance among replicate lines (V d) at F 3 against the expected additive genetic variance among lines (2 F t V A0 , where F t is the coefficient of inbreeding at generation t and V A0 is the additive genetic variance in the base population). This analysis was performed for the first six principal components of the wing character set, and using two series of F t estimates, one obtained from demographic parameters, the other from molecular markers. Overall, V d was slightly less than expected, perhaps as a result of some characters being subject to weak stabilizing selection, but the general picture was one of close concordance with the prediction of the neutral additive model. Plots of phenotypic line means, from the parental generation through to F 3 , illustrate that the observed differentiation was essentially entirely due to the initial sampling event. Egg weight showed a similar pattern of differentiation.
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.
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.
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.
Biological Journal of The Linnean Society, 2006
The consequences of population bottlenecks for morphological differentiation were investigated experimentally in the Afrotropical butterfly Bicyclus anynana (Satyrinae). A genetically variable laboratory population was used to establish daughter populations differing in the severity of the founding bottleneck (two, six, 20 and c. 300 individuals), with four to six replicate lines per treatment. Nine quantitative traits of the hind wing were measured (wing area and eight wing pattern characters) in the founders, F1, F2 and F3 generations. A tenth character, egg weight, was measured in all lines in F3. The validity of the neutral additive model was tested by regressing the observed phenotypic variance among replicate lines (Vd) at F3 against the expected additive genetic variance among lines (2FtVA0, where Ft is the coefficient of inbreeding at generation t and VA0 is the additive genetic variance in the base population). This analysis was performed for the first six principal components of the wing character set, and using two series of Ft estimates, one obtained from demographic parameters, the other from molecular markers. Overall, Vd was slightly less than expected, perhaps as a result of some characters being subject to weak stabilizing selection, but the general picture was one of close concordance with the prediction of the neutral additive model. Plots of phenotypic line means, from the parental generation through to F3, illustrate that the observed differentiation was essentially entirely due to the initial sampling event. Egg weight showed a similar pattern of differentiation. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 89, 107–115.
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.
Proceedings of The Royal Society B: Biological Sciences, 1994
Earlier studies on adaptive plasticity in development time and diapause regulation in the speckled wood butterfly, Pararge aegeria L., have been based on optimality models and have not considered genetics. Nevertheless, they have been successful in predicting patterns observed. From the results of these studies we predicted the genetics of larval and pupal development time, as well as of diapause control, to be polygenic and sex linked. We show that this is the case by crossing a population of the northern subspecies P. a. tircis from southern Sweden, which shows a diapause in some daylengths and is protandrous, with a population of the southern subspecies P. a. aegeria from Madeira. The latter inhabits a much less seasonal environment, develops directly at all daylengths, and is not protandrous. Offspring showed variable and intermediate larval and pupal development times when reared at daylengths inducing diapause in Swedish pure stock. Female offspring were more similar to their mothers in the reciprocal crosses, whereas development time in male offspring was not sensitive to the direction of the cross. This suggests the presence of a sex-linked modifying factor. The results show that the outcome of tests of optimality models can be used to predict genetic systems.
The genetic basis of hindwing eyespot number variation in Bicyclus anynana butterflies
The underlying genetic changes that regulate the appearance and disappearance of repeated traits, or serial homologs, remain poorly understood. One hypothesis is that variation in genomic regions flanking master regulatory genes, also known as input-output genes, controls variation in trait number, making the locus of evolution almost predictable. Other hypotheses implicate genetic variation in up-stream or downstream loci of master control genes. Here, we use the butterfly Bicyclus anynana, a species which exhibits natural variation in eyespot number on the dorsal hindwing, to test these two hypotheses. We first estimated the heritability of dorsal hindwing eyespot number by breeding multiple butterfly families differing in eyespot number, and regressing eyespot number of offspring on mid-parent values. We then estimated the number and identity of independent genetic loci contributing to eyespot number variation by performing a genome-wide association study with restriction site-as...
Heredity, 2004
Evidence of changes in levels of genetic variation in the field is scarce. Theoretically, selection and a bottleneck may lead to the depletion of additive genetic variance (V A ) but not of nonadditive, dominance variance (V D ), although a bottleneck may converse V D to V A . Here we analyse quantitative genetic variation for the Speckled Wood butterfly Pararge aegeria on the island of Madeira about 120 generations after first colonisation. Colonisation of the island involved both a bottleneck and strong natural selection, changing the average value of traits. Several life history and morphological traits with varying levels of change since colonisation were analysed. In accordance with expectations, all traits except one showed relatively low levels of V A , with an average heritability (h 2 ) of 0.078. Levels of V D for these traits were relatively high, 20-94% of total variance and on average 80% of V G . The exception was a morphological trait that probably had not experienced strong natural selection after colonisation, for which a h 2 of 0.27 was found. Another interesting observation is that the population seems resistant to inbreeding effects, which may be the result of purging of deleterious alleles.
Ontogenetic Basis of Among-Generation Differences in Size-Related Traits in a Polyphenic Butterfly
2021
Seasonal polyphenisms are cases in which individuals representing generations occurring in different times of the year systematically differ in their morphological, physiological, and/or behavioral traits. Such differences are often assumed to constitute adaptive responses to seasonally varying environments, but the evidence for this is still scarce. The adaptive character of the response would be corroborated by the pattern in which the decision about choosing a particular seasonal phenotype is made before the onset of respective environmental conditions (anticipatory plasticity). Alternatively, the between-generation differences can be caused by immediate effects of seasonally varying environments (responsive plasticity). Here we reared the larvae of the seasonally polymorphic map butterfly Araschnia levana under two different photoperiodic regimes, which provided different seasonal cues. These two treatments induced direct development and diapause pathways, respectively. Replicat...