Evolutionary Divergence of the Genetic Architecture Underlying Photoperiodism in the Pitcher-Plant Mosquito, Wyeomyia Smithii

We determine the contribution of composite additive, dominance, and epistatic effects to the genetic divergence of photoperiodic response along latitudinal, altitudinal, and longitudinal gradients in the pitcher-plant mosquito, Wyeomyia smithii. Joint scaling tests of crosses between populations showed wide-spread epistasis as well as additive and dominance differences among populations. There were differences due to epistasis between an alpine population in North Carolina and populations in Florida, lowland North Carolina, and Maine. Longitudinal displacement resulted in differences due to epistasis between Florida and Alabama populations separated by 300 km but not between Maine and Wisconsin populations separated by 2000 km. Genetic differences between New Jersey and Ontario did not involve either dominance or epistasis and we estimated the minimum number of effective factors contributing to a difference in mean critical photoperiod of 5 SD between them as n(E) = 5. We propose that the genetic similarity of populations within a broad northern region is due to their more recent origin since recession of the Laurentide Ice Sheet and that the unique genetic architecture of each population is the result of both mutation and repeated migration-founder-flush episodes during the dispersal of W. smithii in North America. Our results suggest that differences in composite additive and dominance effects arise early in the genetic divergence of populations while differences due to epistasis accumulate after more prolonged isolation.     

Population differentiation in the beetleTribolium castaneum. I. Genetic architecture

We used joint-scaling analyses in conjunction with rearing temperature variation to investigate the contributions of additive, non-additive, and environmental effects to genetic divergence and incipient speciation among 12 populations of the red flour beetle, Tribolium castaneum, with small levels of pairwise nuclear genetic divergence (0.033 < Nei's D < 0.125). For 15 population pairs we created a full spectrum of line crosses (two parental, two reciprocal F1's, four F2's, and eight backcrosses), reared them at multiple temperatures, and analyzed the numbers and developmental defects of offspring. We assayed a total of 219,388 offspring from 5147 families. Failed crosses occurred predominately in F2's, giving evidence of F2 breakdown within this species. In all cases where a significant model could be fit to the data on offspring number, we observed at least one type of digenic epistasis. We also found maternal and cytoplasmic effects to be common components of divergence among T. castaneum populations. In some cases, the most complex model tested (additive, dominance, epistatic, maternal, and cytoplasmic effects) did not provide a significant fit to the data, suggesting that linkage or higher order epistasis is involved in differentiation between some populations. For the limb deformity data, we observed significant genotype-by-environment interaction in most crosses and pure parent crosses tended to have fewer deformities than hybrid crosses. Complexity of genetic architecture was not correlated with either geographic distance or genetic distance. Our results support the view that genetic incompatibilities responsible for postzygotic isolation, an important component of speciation, may be a natural but serendipitous consequence of nonadditive genetic effects and structured populations.     

A TEST OF THE ROLE OF EPISTASIS IN DIVERGENCE UNDER UNIFORM SELECTION

Five populations of Drosophila melanogaster have previously been shown to be replicably different in their responses to artificial selection for knockdown resistance to ethanol fumes (Cohan and Hoffmann, 1986). The present study tests whether this divergence could be attributed to the epistatic mechanism assumed by Wright's shifting-balance model of evolution, in which alleles favored in the genetic background of one population are not favored in that of another. If this were the mechanism of divergence, crosses between selected lines from different populations would be expected to yield an epistatic loss of the selected phenotype. However, all such crosses showed a good fit to an additive model with dominance. Divergence by an epistatic mechanism may also be associated with epistatic variance within populations, but no evidence for such epistasis was found. The populations therefore appear to have responded in different ways to selection not because of epistasis but because knockdown-resistance alleles that were common in some populations were absent (or at least less common) in others.     

The contrasting genetic architecture of wing size, viability, and development time in a rainforest species and its more widely distributed relative

Divergence among populations can occur via additive genetic effects and/or because of epistatic interactions among genes. Here we use line-cross analysis to compare the importance of epistasis in divergence among two sympatric Drosophila species from eastern Australia, one (D. serrata) distributed continuously and the other (D. birchii) confined to rainforest habitats that are often disjunct. For D. serrata, crosses indicated that development time and wing size differences were due to additive genetic effects, while for viability there were digenic epistatic effects. Crosses comparing geographically close populations as well as those involving the most geographically distant populations (including the southern species border) revealed epistatic interactions, whereas crosses at an intermediate distance showed no epistasis. In D. birchii, there was no evidence of epistasis for viability, although for development time and wing size there was epistasis in the cross between the most geographically diverged populations. Strong epistasis has not developed among the D. birchii populations, and this habitat specialist does not show stronger epistasis than D. serrata. Given that epistasis has been detected in crosses with other species from eastern Australia, including the recently introduced D. melanogaster, the results point to epistasis not being directly linked to divergence times among populations.     

The mapping of epistatic effects onto a genealogical tree in haploid populations

In this paper we present a model that maps epistatic effects onto a genealogical tree for a haploid population. Prior work has demonstrated that genealogical structure causes the genotypic values of individuals to covary. Our results indicate that epistasis can reduce genotypic covariance that is caused by genealogical structure. Genotypic effects (both additive and epistatic) occur along the branches of a genealogical tree, from the base of the tree to its tips. Epistasis reduces genotypic covariance because there is a reweighting of the contribution of branches to the states of genotypes compared to the additive case. Branches near the tips of a genealogical tree contribute proportionally more genetic effects with epistasis than without epistasis. Epistatic effects are most numerous at basal positions in a genealogical tree when a population is constant in size and experiencing no selection, optimizing selection, diversifying selection or directional selection, indicating that epistatic effects are typically old. For a population that is growing in size, epistatic effects are most numerous at midpoints in a genealogical tree, indicating epistatic effects are of moderate age. Our results are important in that they suggest epistatic effects may typically explain deep (old) divergences and broad patterns of divergence that exist in populations, except in growing populations. In a growing population, epistatic effects may cause more within group divergence higher up in a tree and less between group divergence that is deep in a tree. The distribution of the number of epistatic effects and the expected variance and covariance in the number of epistatic effects is also provided assuming neutrality.     

A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster

Body size clines in Drosophila melanogaster have been documented in both Australia and South America, and may exist in Southern Africa. We crossed flies from the northern and southern ends of each of these clines to produce F(1), F(2), and first backcross generations. Our analysis of generation means for wing area and wing length produced estimates of the additive, dominance, epistatic, and maternal effects underlying divergence within each cline. For both females and males of all three clines, the generation means were adequately described by these parameters, indicating that linkage and higher order interactions did not contribute significantly to wing size divergence. Marked differences were apparent between the clines in the occurrence and magnitude of the significant genetic parameters. No cline was adequately described by a simple additive-dominance model, and significant epistatic and maternal effects occurred in most, but not all, of the clines. Generation variances were also analyzed. Only one cline was described sufficiently by a simple additive variance model, indicating significant epistatic, maternal, or linkage effects in the remaining two clines. The diversity in genetic architecture of the clines suggests that natural selection has produced similar phenotypic divergence by different combinations of gene action and interaction.     

Chromosomal basis of viability differences in Tigriopus californicus interpopulation hybrids

Crosses between populations of Tigriopus californicus result in backcross and F2 hybrid breakdown for a variety of fitness related measures. The magnitude of this hybrid breakdown is correlated with evolutionary divergence. We assessed the chromosomal basis of viability differences in nonrecombinant backcross hybrids using markers mapped to individual chromosomes. To assess effects of evolutionary divergence we crossed one population to three different populations: two distantly related (approximately 18% mitochondrial COI sequence divergence) and one closely related (approximately 1% mitochondrial COI sequence divergence). We found that all three interpopulation crosses resulted in significant deviations from expected Mendelian ratios at a majority of the loci studied. In all but one case, deviations were due to a deficit of parental homozygotes. This pattern implies that populations of T. californicus carry a significant genetic load, and that a combination of beneficial dominance and deleterious homozygote-heterozygote interactions significantly affects hybrid viability. Pairwise tests of linkage disequilibrium detected relatively few significant interactions. For the two divergent crosses, effects of individual chromosomes were highly concordant. These two crosses also showed higher heterozygote excess in females than males across the vast majority of chromosomes.     

Population bottlenecks increase additive genetic variance but do not break a selection limit in rain forest Drosophila

According to neutral quantitative genetic theory, population bottlenecks are expected to decrease standing levels of additive genetic variance of quantitative traits. However, some empirical and theoretical results suggest that, if nonadditive genetic effects influence the trait, bottlenecks may actually increase additive genetic variance. This has been an important issue in conservation genetics where it has been suggested that small population size might actually experience an increase rather than a decrease in the rate of adaptation. Here we test if bottlenecks can break a selection limit for desiccation resistance in the rain forest-restricted fly Drosophila bunnanda. After one generation of single-pair mating, additive genetic variance for desiccation resistance increased to a significant level, on average higher than for the control lines. Line crosses revealed that both dominance and epistatic effects were responsible for the divergence in desiccation resistance between the original control and a bottlenecked line exhibiting increased additive genetic variance for desiccation resistance. However, when bottlenecked lines were selected for increased desiccation resistance, there was only a small shift in resistance, much less than predicted by the released additive genetic variance. The small selection response in the bottlenecked lines was no greater than that observed in the control lines. Thus bottlenecks might produce a statistically detectable change in additive genetic variance but this change has no impact on the response to selection.     

Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice using advanced backcross progeny

A backcrossed population (BC(4)F(2)) derived from a cross between a japonica rice variety, Nipponbare, as the recurrent parent and an indica rice variety, Kasalath, as the donor parent showed a long-range variation in days to heading. Quantitative trait loci (QTL) analysis revealed that two QTL, one on chromosome 3, designated Hd6, and another on chromosome 2, designated Hd7, were involved in this variation; and Hd6 was precisely mapped as a single Mendelian factor by using progeny testing (BC(4)F(3)). The nearly isogenic line with QTL (QTL-NIL) that carries the chromosomal segment from Kasalath for the Hd6 region in Nipponbare's genetic background was developed by marker-assisted selection. In a day-length treatment test, the QTL-NIL for Hd6 prominently increased days to heading under a 13.5-hr day length compared with the recurrent parent, Nipponbare, suggesting that Hd6 controls photoperiod sensitivity. QTL analysis of the F(2) population derived from a cross between the QTL-NILs revealed existence of an epistatic interaction between Hd2, which is one of the photoperiod sensitivity genes detected in a previous analysis, and Hd6. The day-length treatment tests of these QTL-NILs, including the line introgressing both Hd2 and Hd6, also indicated an epistatic interaction for photoperiod sensitivity between them.     

Genetics of behavioural and morphological differences between parapatric subspecies of Chorthippus parallelus (Orthoptera: Acrididae)

The grasshoppers Chorthippus parallelus parallelus and C. p. erythropus form a narrow hybrid zone in the Pyrenees. They differ in several characters of the pattern and structure of male stridulation and in the morphology of the stridulatory file. These characters are considered to be involved in the species' mate recognition system.
Crosses have been made between a Pyrenean C. p. erythropus population and two C. p. parallelus populations, one in the Pyrenees and one in the Massif Central. Reciprocal Fls and backcrosses have been examined for a set of stridulation and associated morphological characters. The crosses confirm that the subspecific differences have a genetic basis and suggest that they are polygenically determined. However the mode of inheritance is not simple. There is evidence for dominance and epistatic effects and for sex-linkage or maternal effects. Genetic correlations exist between some pairs of characters in the backcrosses.
These results are discussed in the context of the hybrid zone and in relation to the general problem of the evolutionary divergence of mate recognition systems.     

Population differentiation in an annual legume: genetic architecture

Abstract. The presence or absence of epistasis, or gene interaction, is explicitly assumed in many evolutionary models. Although many empirical studies have documented a role of epistasis in population divergence under laboratory conditions, there have been very few attempts at quantifying epistasis in the native environment where natural selection is expected to act. In addition, we have little understanding of the frequency with which epistasis contributes to the evolution of natural populations. In this study we used a quantitative genetic design to quantify the contribution of epistasis to population divergence for fitness components of a native annual legume, Chamaecrista fasciculata . The design incorporated the contrast of performance of F₂ and F₃ segregating progeny of 18 interpopulation crosses with the F₁ and their parents. Crosses were conducted between populations from 100 m to 2000 km apart. All generations were grown for two seasons in the natural environment of one of the parents. The F₁ often outperformed the parents. This F₁ heterosis reveals population structure and suggests that drift is a major contributor to population differentiation. The F₂ generation demonstrated that combining genes from different populations can sometimes have unexpected positive effects. However, the F₃ performance indicated that combining genes from different populations decreased vigor beyond that due to the expected loss of heterozygosity. Combined with previous data, our results suggest that both selection and drift contribute to population differentiation that is based on epistatic genetic divergence. Because only the F₃ consistently expressed hybrid breakdown, we conclude that the epistasis documented in our study reflects interactions among linked loci.     

The quantitative genetic basis of adaptive divergence in the moor frog (Rana arvalis) and its implications for gene flow

Knowledge on the relative contribution of direct genetic, maternal and environmental effects to adaptive divergence is important for understanding the drivers of biological diversification. The moor frog (Rana arvalis) shows adaptive divergence in embryonic and larval fitness traits along an acidification gradient in south-western Sweden. To understand the quantitative genetic basis of this divergence, we performed reciprocal crosses between three divergent population pairs and reared embryos and larvae at acid and neutral pH in the laboratory. Divergence in embryonic acid tolerance (survival) was mainly determined by maternal effects, whereas the relative contributions of maternal, additive and nonadditive genetic effects in larval life-history traits differed between traits, population pairs and rearing environments. These results emphasize the need to investigate the quantitative genetic basis of adaptive divergence in multiple populations and traits, as well as different environments. We discuss the implications of our findings for maintenance of local adaptation in the context of migrant and hybrid fitness.     

A quantitative genetic analysis of nuclear-cytoplasmic male sterility in structured populations of Silene vulgaris

Gynodioecy, the coexistence of functionally female and hermaphroditic morphs within plant populations, often has a complicated genetic basis involving several cytoplasmic male-sterility factors and nuclear restorers. This complexity has made it difficult to study the genetics and evolution of gynodioecy in natural populations. We use a quantitative genetic analysis of crosses within and among populations of Silene vulgaris to partition genetic variance for sex expression into nuclear and cytoplasmic components. We also use mitochondrial markers to determine whether cytoplasmic effects on sex expression can be traced to mitochondrial variance. Cytoplasmic variation and epistatic interactions between nuclear and cytoplasmic loci accounted for a significant portion of the variation in sex expression among the crosses. Source population also accounted for a significant portion of the sex ratio variation. Crosses among populations greatly enhanced the dam (cytoplasmic) effect, indicating that most among-population variance was at cytoplasmic loci. This is supported by the large among-population variance in the frequency of mitochondrial haplotypes, which also accounted for a significant portion of the sex ratio variance in our data. We discuss the similarities between the population structure we observed at loci that influence sex expression and previous work on putatively neutral loci, as well as the implications this has for what mechanisms may create and maintain population structure at loci that are influenced by natural selection.     

Quantitative genetics of functional characters in<Emphasis Type="Italic">Drosophila melanogaster</Emphasis> populations subjected to laboratory selection

What are the genetics of phenotypes other than fitness, in outbred populations? To answer this question, the quantitative-genetic basis of divergence was characterized for outbredDrosophila melanogaster populations that had previously undergone selection to enhance characters related to fitness. Line-cross analysis using first-generation and second-generation hybrids from reciprocal crosses was conducted for two types of cross, each replicated fivefold. One type of cross was between representatives of the ancestral population, a set of five populations maintained for several hundred generations on a two-week discrete-generation life cycle and a set of five populations adapted to starvation stress. The other type of cross was between the same set of ancestral-representative populations and another set of five populations selected for accelerated development from egg to egg. Developmental time from egg to eclosion, starvation resistance, dry body weight and fecundity at day 14 from egg were fit to regression models estimating single-locus additive and dominant effects, maternal and paternal effects, and digenic additive and dominance epistatic effects. Additive genetic variation explained most of the differences between populations, with additive maternal and cytoplasmic effects also commonly found. Both within-locus and between-locus dominance effects were inferred in some cases, as well as one instance of additive epistasis. Some of these effects may have been caused by linkage disequilibrium. We conclude with a brief discussion concerning the relationship of the genetics of population differentiation to adaptation.     

Evolution of stickleback feeding behaviour: genetics of population divergence at different ontogenetic stages

The evolutionary significance of individual consistency in a given behaviour – called animal personality – has been subject to a lot of recent research. However, the genetic underpinnings of population divergence in mean personality have rarely been studied, especially across different ontogenetic stages. Previous work has shown that marine vs. pond populations of nine‐spined sticklebacks (Pungitius pungitius) have undergone adaptive divergence in a series of fitness‐related traits, including behaviour. One particular behavioural trait important in this system is feeding activity: giant pond sticklebacks are more active feeders than their normal sized marine conspecifics. In a common garden experiment, we raised individuals from pure and hybrid F₁‐generation crosses of a highly divergent marine – pond population pair to see if (i) feeding activity and/or its ontogenetic change was consistent between individuals, and if (ii) population divergence at different ontogenetic stages could be explained by additive genetic, nonadditive genetic or maternal effects. We found that feeding activity decreased with age, but that these changes were consistently different among both individuals and crosses. The among cross patterns were consistent with a nonadditive genetic scenario: in the early period pond sticklebacks expressed dominance for high feeding activity, while in the late period marine sticklebacks expressed dominance for low feeding activity. We conclude that nine‐spined sticklebacks exhibit different feeding personalities, and that the population divergence in feeding personality is explainable by age‐dependent expression of genetic dominance.     

Evolutionary divergence in thermal sensitivity and diapause of field and laboratory populations of manduca sexta

The tobacco hornworm Manduca sexta has been an important model system in insect biology for more than half a century. Here we report the evolutionary divergence in thermal sensitivity and diapause initiation between field and laboratory populations that were separated for more than 35 yr (>240 laboratory generations) and that are descendants from the same field populations in central North Carolina. At intermediate rearing temperatures (20 degrees-25 degrees C), mean body size was significantly larger and development time significantly faster in the laboratory than in the field populations. At higher temperatures (30 degrees -35 degrees C), these mean differences between populations were reduced or eliminated, and larval survival at 35 degrees C was significantly lower in the laboratory population than in the field population. F(1) crosses had survival and development time to wandering similar to the field population times at both 25 degrees and 35 degrees C; body mass at wandering for F(1) crosses was intermediate compared with that of the field and laboratory populations. Comparisons with earlier field and laboratory studies suggest evolutionary reductions in thermal tolerance and performance at high temperatures in the laboratory population. The critical photoperiod initiating diapause in field populations in North Carolina did not change detectably between the 1960s and 2005. In contrast, the laboratory population has evolved a reduced tendency to diapause under short-day conditions, relative to the field population.     

The effect of genetic drift on the variance/covariance components generated by multilocus additive x additive epistatic systems

The effect of population bottlenecks on the components of the genetic variance/covariance generated by n neutral independent additive x additive loci has been studied theoretically. In its simplest version, this situation can be modelled by specifying the allele frequencies and homozygous effects at each locus, and an additional factor measuring the strength of the n-th order epistatic interaction. The variance/covariance components in an infinitely large panmictic population (ancestral components) were compared with their expected values at equilibrium over replicates randomly derived from the base population, after t bottlenecks of size N (derived components). Formulae were obtained giving the derived components (and the between-line variance) as functions of the ancestral ones (alternatively, in terms of allele frequencies and effects) and the corresponding inbreeding coefficient F(t). The n-th order derived component of the genetic variance/covariance is continuously eroded by inbreeding, but the remaining components may increase initially until a critical F(t) value is attained, which is inversely related to the order of the pertinent component, and subsequently decline to zero. These changes can be assigned to the between-line variances/covariances of gene substitution and epistatic effects induced by drift. Numerical examples indicate that: (1) the derived additive variance/covariance component will generally exceed its ancestral value unless epistasis is weak; (2) the derived epistatic variance/covariance components will generally exceed their ancestral values unless allele frequencies are extreme; (3) for systems showing equal ancestral additive and total non-additive variance/covariance components, those including a smaller number of epistatic loci may generate a larger excess in additive variance/covariance after bottlenecks than others involving a larger number of loci, provided that F(t) is low. Our results indicate that it is unlikely that the rate of evolution may be significantly accelerated after population bottlenecks, in spite of occasional increments of the derived additive variance over its ancestral value.     

Nonadditive genetic components in resistance of the red flour beetle Tribolium castanaeum against parasite infection

Genetically coupled antagonistic coevolution between host and parasites can select for the maintenance of recombination in the host. Mechanistically, maintenance of recombination relies on epistatic interactions between resistance genes creating linkage disequilibria (LD). The role of epistasis in host resistance traits is however only partly understood. Therefore, we applied the joint scaling principle to assess epistasis and other nonadditive genetic components of two resistance traits, survival, and parasite spore load, in population crosses of the red flour beetle Tribolium castanaeum under infections with the microsporidian Nosema whitei. We found nonadditive components only in infected populations but not in control populations. The genetic architecture underlying survival under parasite infection was more complex than that of spore load. Accordingly, the observed negative correlation between survival and spore load was mainly based on a correlation between shared additive components. Breakdown of resistance was especially strong in F2 crosses between resistant lines indicating that multiple epistatic routes can lead to the same adaptation. In general, the wide range of nonoverlapping genetic components between crosses indicated that parasite resistance in T. castanaeum can be understood as a multi peaked fitness landscape with epistasis contributing substantially to phenotypic differentiation in resistance.     

Epistatic pleiotropy and the genetic architecture of covariation within early and late-developing skull trait complexes in mice

The role of epistasis as a source of trait variation is well established, but its role as a source of covariation among traits (i.e., as a source of "epistatic pleiotropy") is rarely considered. In this study we examine the relative importance of epistatic pleiotropy in producing covariation within early and late-developing skull trait complexes in a population of mice derived from an intercross of the Large and Small inbred strains. Significant epistasis was found for several pairwise combinations of the 21 quantitative trait loci (QTL) affecting early developing traits and among the 20 QTL affecting late-developing traits. The majority of the epistatic effects were restricted to single traits but epistatic pleiotropy still contributed significantly to covariances. Because of their proportionally larger effects on variances than on covariances, epistatic effects tended to reduce within-group correlations of traits and reduce their overall degree of integration. The expected contributions of single-locus and two-locus epistatic pleiotropic QTL effects to the genetic covariance between traits were analyzed using a two-locus population genetic model. The model demonstrates that, for single-locus or epistatic pleiotropy to contribute to trait covariances in the study population, both traits must show the same pattern of single-locus or epistatic effects. As a result, a large number of the cases where loci show pleiotropic effects do not contribute to the covariance between traits in this population because the loci show a different pattern of effect on the different traits. In general, covariance patterns produced by single-locus and epistatic pleiotropy predicted by the model agreed well with actual values calculated from the QTL analysis. Nearly all single-locus and epistatic pleiotropic effects contributed positive components to covariances between traits, suggesting that genetic integration in the skull is achieved by a complex combination of pleiotropic effects.     

The genetic basis of flowering time and photoperiod sensitivity in rapeseed (Brassica napus L.)

The objective of this study was to dissect the genetic control of days to flowering (DTF) and photoperiod sensitivity (PS) into the various components including the main-effect quantitative trait loci (QTLs), epistatic QTLs and QTL-by-environment interactions (QEs). Doubled haploid (DH) fines were produced from an F1 between two spring Brassica napus cultivars Hyola 401 and Q2. DTF of the DH lines and parents were investigated in two locations, one location with a short and the other with a long photoperiod regime over two years. PS was calculated by the delay in DTF under long day as compared to that under short day. A genetic linkage map was constructed that comprised 248 marker loci including SSR, SRAP and AFLP markers. Further QTL analysis resolved the genetic components of flowering time and PS into the main-effect QTLs, epistatic QTLs and QEs. A total of 7 main-effect QTLs and 11 digenic interactions involving 21 loci located on 13 out of the 19 linkage groups were detected for the two traits. 3 main-effect QTLs and 4 pairs of epistatic QTLs were involved in QEs conferring DTF. One QTL on linkage group (LG) 18 was revealed to simultaneously affect DTF and PS and explain for the highest percentage of the phenotypic variation. The implications of the results for B. napus breeding have been discussed.