Heterosis is common and inbreeding depression absent in natural populations of Arabidopsis thaliana

The importance of genetic drift in shaping patterns of adaptive genetic variation in nature is poorly known. Genetic drift should drive partially recessive deleterious mutations to high frequency, and inter‐population crosses may therefore exhibit heterosis (increased fitness relative to intra‐population crosses). Low genetic diversity and greater genetic distance between populations should increase the magnitude of heterosis. Moreover, drift and selection should remove strongly deleterious recessive alleles from individual populations, resulting in reduced inbreeding depression. To estimate heterosis, we crossed 90 independent line pairs of Arabidopsis thaliana from 15 pairs of natural populations sampled across Fennoscandia and crossed an additional 41 line pairs from a subset of four of these populations to estimate inbreeding depression. We measured lifetime fitness of crosses relative to parents in a large outdoor common garden (8,448 plants in total) in central Sweden. To examine the effects of genetic diversity and genetic distance on heterosis, we genotyped parental lines for 869 SNPs. Overall, genetic variation within populations was low (median expected heterozygosity = 0.02), and genetic differentiation was high (median F_ST = 0.82). Crosses between 10 of 15 population pairs exhibited significant heterosis, with magnitudes of heterosis as high as 117%. We found no significant inbreeding depression, suggesting that the observed heterosis is due to fixation of mildly deleterious alleles within populations. Widespread and substantial heterosis indicates an important role for drift in shaping genetic variation, but there was no significant relationship between fitness of crosses relative to parents and genetic diversity or genetic distance between populations.     

Investigating the genetic load of an emblematic invasive species: the case of the invasive harlequin ladybird Harmonia axyridis

Introduction events can lead to admixture between genetically differentiated populations and bottlenecks in population size. These processes can alter the adaptive potential of invasive species by shaping genetic variation, but more importantly, they can also directly affect mean population fitness either increasing it or decreasing it. Which outcome is observed depends on the structure of the genetic load of the species. The ladybird Harmonia axyridis is a good example of invasive species where introduced populations have gone through admixture and bottleneck events. We used laboratory experiments to manipulate the relatedness among H. axyridis parental individuals to assess the possibility for heterosis or outbreeding depression in F₁ generation offspring for two traits related to fitness (lifetime performance and generation time). We found that inter‐populations crosses had no major impact on the lifetime performance of the offspring produced by individuals from either native or invasive populations. Significant outbreeding depression was observed only for crosses between native populations for generation time. The absence of observed heterosis is indicative of a low occurrence of fixed deleterious mutations within both the native and invasive populations of H. axyridis. The observed deterioration of fitness in native inter‐population crosses most likely results from genetic incompatibilities between native genomic backgrounds. We discuss the implications of these results for the structure of genetic load in H. axyridis in the light of the available information regarding the introduction history of this species.     

EVOLUTION OF THE GENETIC ARCHITECTURE UNDERLYING FITNESS IN THE PITCHER-PLANT MOSQUITO,WYEOMYIA SMITHII

We examined the genetic basis for evolutionary divergence among geographic populations of the pitcher-plant mosquito, Wyeomyia smithii, using protein electrophoresis and line-cross analysis. Line-cross experiments were performed under both low density, near-optimal conditions, and at high, limiting larval densities sufficient to reduce fitness (r_c) in parental populations by approximately 50%. We found high levels of electrophoretic divergence between ancestral and derived populations, but low levels of divergence between two ancestral populations and between two derived populations. Assessed under near-optimal conditions, the genetic divergence of fitness (r_c) between ancestral and derived populations, but not between two derived populations or between two ancestral populations, has involved both allelic (dominance) and genic (epistatic) interactions. The role of dominance and epistasis in the divergence of r_c among populations affects its component traits in a pattern that is unique to each cross. Patterns of genetic differentiation among populations of W. smithii provide evidence for a topographically complex “adaptive landscape” as envisioned by Wright in his “shifting balance” theory of evolution. Although we cannot definitively rule out the role of deterministic evolution in the divergence of populations on this landscape, ecological inference and genetic data are more consistent with a stochastic than a deterministic process. At high, limiting larval density, hybrid vigor is enhanced and the influence of epistasis disappears. Thus, under stressful conditions, the advantages to fitness due to hybrid heterozygosity can outweigh the deleterious effects of fragmented gene complexes. These results have important implications for the management of inbred populations. Outbreeding depression assessed in experimental crosses under benign lab, zoo, or farm conditions may not accurately reveal the increased advantages of heterozygosity in suboptimal or marginal conditions likely to be found in nature.     

Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata

Genetic incompatibilities and low offspring fitness are characteristic outcomes of hybridization between species. Yet, the creative potential of recombination following hybridization continues to be debated. Here we quantify the outcome of hybridization and recombination between adaptively divergent populations of the North American legume Chamaecrista fasciculata in a large-scale field experiment. Previously, hybrids between these populations demonstrated hybrid breakdown, suggesting the expression of adaptive epistatic interactions underlying population genetic differentiation. However, the outcome of hybridization ultimately rests on the performance of even later generation recombinants. In experiments that compared the performance of recombinant F6 and F2 generations with nonrecombinant F1 and parental genotypes, we observed that increasing recombination had contrasting effects on different life-history components. Lifetime fitness, defined as the product of survivorship and reproduction, showed a strong recovery of fitness in the F6. The overall gain in fitness with increased recombination suggests that hybridization and recombination may provide the necessary genetic variation for adaptive evolution within species. We discuss the mechanisms that may account for the gain in fitness with recombination, and explore the implications for hybrid speciation and phenotypic evolution.     

Population differentiation in an annual legume: local adaptation

Abstract. Studies of many plants species have demonstrated adaptive genetic differentiation to local environmental conditions. Typically these studies are conducted to evaluate adaptation to contrasting environments. As a consequence, although local adaptation has been frequently demonstrated, we have little information as to the spatial scale of adaptive evolution. We evaluated adaptive differentiation between populations of the annual legume Chamaecrista fasciculata using a replicated common-garden design. Study sites were established in three field locations that are home to native populations of C. fasciculata . Each location was planted for two years with seed from the population native to the study site (home population) and populations located six distances (0.1-2000 km) from each site (transplanted populations). Seeds were planted into the study sites with minimum disturbance to determine the scale of local adaptation, as measured by a home-site fitness advantage, for five fitness components: germination, survival, vegetative biomass, fruit production, and the number of fruit produced per seed planted (an estimate of cumulative fitness). For all characters there was little evidence for local adaptation, except at the furthest spatial scales. Patterns of adaptive differentiation were fairly consistent in two of the three sites, but varied between years. Little genetic variation was expressed at the third site. These results, combined with previous estimates of limited gene flow, suggest that metapopulation processes and temporal environmental variation act together to reduce local adaptation, except over long distances.     

Source population characteristics affect heterosis following genetic rescue of fragmented plant populations

Understanding the relative importance of heterosis and outbreeding depression over multiple generations is a key question in evolutionary biology and is essential for identifying appropriate genetic sources for population and ecosystem restoration. Here we use 2455 experimental crosses between 12 population pairs of the rare perennial plant Rutidosis leptorrhynchoides (Asteraceae) to investigate the multi-generational (F₁, F₂, F₃) fitness outcomes of inter-population hybridization. We detected no evidence of outbreeding depression, with inter-population hybrids and backcrosses showing either similar fitness or significant heterosis for fitness components across the three generations. Variation in heterosis among population pairs was best explained by characteristics of the foreign source or home population, and was greatest when the source population was large, with high genetic diversity and low inbreeding, and the home population was small and inbred. Our results indicate that the primary consideration for maximizing progeny fitness following population augmentation or restoration is the use of seed from large, genetically diverse populations.     

Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia)

We studied heterosis and outbreeding depression among immigrants and their descendants in a population of song sparrows on Mandarte Island, Canada. Using data spanning 19 generations, we compared survival, seasonal reproductive success, and lifetime reproductive success of immigrants, natives (birds with resident-hatched parents and grandparents), and their offspring (F1s, birds with an immigrant and a native parent, and F2s, birds with an immigrant grandparent and resident-hatched grandparent in each of their maternal and paternal lines). Lifetime reproductive success of immigrants was no worse than that of natives, but other measures of performance differed in several ways. Immigrant females laid later and showed a tendency to lay fewer clutches, but had relatively high success raising offspring per egg produced. The few immigrant males survived well but were less likely to breed than native males of the same age that were alive in the same year. Female F1s laid earlier than expected based on the average for immigrant and native females, and adult male F1s were more likely to breed than expected based on the average for immigrant and native males. The performance differences between immigrant and native females and between F1s and the average of immigrants and natives are consistent with the hypothesis that immigrants were disadvantaged by a lack of site experience and that immigrant offspring benefited from heterosis. However, we could not exclude the possibility that immigrants had a different strategy for optimizing reproductive success or that they experienced ecological compensation for life-history parameters. For example, the offspring of immigrants may have survived well because immigrants laid later and produced fewer clutches, thereby raising offspring during a period of milder climatic conditions. Although sample sizes were small, we found large performance differences between F1s and F2s, which suggested that either heterosis was associated with epistasis in F1s, that F2s experienced outbreeding depression, or that both phenomena occurred. These findings indicate that the performance of dispersers may be affected more by fine-scale genetic differentiation than previously assumed in this and comparable systems.     

Pollen source affects female reproductive success and early offspring traits in the rare endemic plant Polemonium vanbruntiae (Polemoniaceae)

Understanding the relative magnitudes of inbreeding and outbreeding depression in rare plant populations is increasingly important for effective management strategies. There may be positive and negative effects of crossing individuals in fragmented populations. Conservation strategies may include introducing new genetic material into rare plant populations, which may be beneficial or detrimental based on whether hybrid offspring are of increased or decreased quality. Thus, it is important to determine the effects of pollen source on offspring fitness in rare plants. We established pollen crosses (i.e. geitonogamous‐self, autonomous‐self, intrasite‐outcross, intersite‐outcross and open‐pollinated controls) to determine the effects of pollen source on fitness (seeds/fruit and seed mass) and early offspring traits (probability of germination, number of leaves, leaf area and seedling height) in the rare plant Polemonium vanbruntiae. Open‐pollinated, intrasite‐outcross and geitonogamous‐self treatments did not differ in fitness. However, plants receiving autonomous‐self pollen had the lowest fitness and the lowest probability of seed germination. Intersite‐outcross plants contained fewer seeds/fruit, but seeds germinated at higher frequencies and seedlings were more vigorous. We also detected heterosis at the seed germination stage. These data may imply that natural populations of P. vanbruntiae exhibit low genetic variation and little gene flow. Evidence suggests that deleterious alleles were not responsible for reduced germination; rather environmental factors, dichogamy, herkogamy and/or lack of competition among pollen grains may have caused low germinability in selfed offspring. Although self‐pollination may provide some reproductive assurance in P. vanbruntiae, the result is a reduction in germination and size‐related early traits for selfed offspring.     

Genetic rescue of small inbred populations: meta‐analysis reveals large and consistent benefits of gene flow

Many species have fragmented distribution with small isolated populations suffering inbreeding depression and/or reduced ability to evolve. Without gene flow from another population within the species (genetic rescue), these populations are likely to be extirpated. However, there have been only ~ 20 published cases of such outcrossing for conservation purposes, probably a very low proportion of populations that would potentially benefit. As one impediment to genetic rescues is the lack of an overview of the magnitude and consistency of genetic rescue effects in wild species, I carried out a meta‐analysis. Outcrossing of inbred populations resulted in beneficial effects in 92.9% of 156 cases screened as having a low risk of outbreeding depression. The median increase in composite fitness (combined fecundity and survival) following outcrossing was 148% in stressful environments and 45% in benign ones. Fitness benefits also increased significantly with maternal ΔF (reduction in inbreeding coefficient due to gene flow) and for naturally outbreeding versus inbreeding species. However, benefits did not differ significantly among invertebrates, vertebrates and plants. Evolutionary potential for fitness characters in inbred populations also benefited from gene flow. There are no scientific impediments to the widespread use of outcrossing to genetically rescue inbred populations of naturally outbreeding species, provided potential crosses have a low risk of outbreeding depression. I provide revised guidelines for the management of genetic rescue attempts.     

The evolution of genetic architecture. I. Diversification of genetic backgrounds by genetic drift

The genetic architecture of a phenotype plays a critical role in determining phenotypic evolution through its effects on patterns of genetic variation. Genetic architecture is often considered to be constant in evolutionary quantitative genetic models. However, genetic architecture may be variable and itself evolve when there are dominance and epistatic interactions among alleles at the same and different loci, respectively. The evolution of genetic architecture by genetic drift is examined here by testing the breeding value of four standard inbred mouse strains mated across a set of 26 related recombinant quasi-inbred (RqI) lines generated from the intercross of the Large (LG/J) and Small (SM/J) inbred mouse strains. Phenotypes of interest include age-specific body weights, growth, and adult body composition. If the genetic architecture of these traits has differentiated by genetic drift during the production of the RqI strains, we should observe interactions between tester strain and RqI strain. The breeding values of the tester strains will change relative to one another depending on which RqI strain they are crossed to. The study included an average of 15.1 offspring per cross, over a total of 100 different crosses. Multivariate and univariate analyses of variance indicate that there is strongly significant interaction for all traits. Interaction is more pronounced in males than in females and accounted for an average of about 40% of the explained variation in males and 30% in females. These results indicate that the genetic architecture of these traits has differentiated by genetic drift in the RqI strains since their isolation from a common founder population. Further analysis indicates that this differentiation results in changes in the order of tester strain effects so that common patterns of selection in these differentiated populations could result in the fixation of different alleles.     

Population size and the nature of genetic load in Gentianella germanica

Abstract Theory predicts a significant relationship between the size of a population and the magnitude and composition of its genetic load, but few natural populations have been investigated. We examined the magnitude of genetic load due to recessive deleterious alleles (GL) both segregating and fixed within Gentianella germanica populations of varying size by selfing and reciprocally crossing plants within and between natural populations according to a partial diallel design and by comparing the performance of the experimental progeny in a common-garden experiment. The results show that GL for total fitness in small populations (fewer than 200 plants) was mainly due to fixed recessive deleterious alleles, whereas GL for total fitness in larger populations (more than 200 plants) appeared to be mainly due to segregating deleterious recessive alleles. The total fitness of selfed plants increased with decreasing population size, indicating some purging of deleterious alleles associated with declining population sizes. The magnitudes of GL due to fixed deleterious alleles in small populations and segregating deleterious alleles in large populations, however, were overall similar, suggesting that purging selection was an insignificant force when compared to genetic drift in determining the magnitude of GL in small natural populations in this species. The results of this study highlight the importance of population size in determining the dynamics of genetic loads of natural populations and are overall in line with a large body of theoretical work indicating that small populations may face higher extinction risks due to the fixation and accumulation of deleterious alleles of small effect.     

Inbreeding depression and low between-population heterosis in recently diverged experimental populations of a selfing species

In fragmented populations, genetic drift and selection reduce genetic diversity, which in turn results in a loss of fitness or in a loss of evolvability. Genetic rescue, that is, controlled input of diversity from distant populations, may restore evolutionary potential, whereas outbreeding depression might counteract the positive effect of this strategy. We carried out self-pollination and crosses within and between populations in an experimental subdivided population of a selfing species, Triticum aestivum L., to estimate the magnitude of these two phenomena. Surprisingly, for a self-fertilizing species, we found significant inbreeding depression within each population for four of the six traits studied, indicating that mildly deleterious mutations were still segregating in these populations. The progeny of within- and between-population crosses was very similar, indicating low between-population heterosis and little outbreeding depression. We conclude that relatively large population effective sizes prevented fixation of a high genetic load and that local adaptation was limited in these recently diverged populations. The kinship coefficient estimated between the parents using 20 neutral markers was a poor predictor of the progeny phenotypic values, indicating that there was a weak link between neutral diversity and genes controlling fitness-related traits. These results show that when assessing the viability of natural populations and the need for genetic rescue, the use of neutral markers should be complemented with information about the presence of local adaptation in the subdivided population.     

Severe outbreeding and inbreeding depression maintain mating system differentiation in Epipactis (Orchidaceae)

In hermaphroditic plants, theory for mating system evolution predicts that populations will evolve to either complete autonomous selfing (AS) or complete outcrossing, depending on the balance between automatic selection favouring self‐fertilization and costs resulting from inbreeding depression (ID). Theory also predicts that selection for selfing can occur rapidly and is driven by purging of genetic load and the loss of ID. Therefore, selfing species are predicted to have low levels of ID or even to suffer from outbreeding depression (OD), whereas predominantly outcrossing species are expected to have high levels of ID. To test these predictions, we related the capacity of AS to the magnitude of early‐acting inbreeding or OD in both allogamous and autogamous species of the orchid genus Epipactis. For each species, the level of AS was assessed under controlled greenhouse conditions, whereas hand‐pollinations were performed to quantify early costs of inbreeding or OD acting at the level of fruit and seed production. In the autogamous species, the capacity of AS was high (> 0.72), whereas in the allogamous species AS was virtually absent (< 0.10). Consistent with our hypothesis, allogamous Epipactis species had significantly higher total ID (average: 0.46) than autogamous species, which showed severe costs of OD (average: ?0.45). Overall, our findings indicate that strong early‐acting ID represents an important mechanism that contributes to allogamy in Epipactis, whereas OD may maintain selfing in species that have evolved to complete selfing.     

Genetic architecture of differences between populations of cowpea weevil (Callosobruchus maculatus) evolved in the same environment

We investigated the genetic architecture underlying differentiation in fitness-related traits between two pairs of populations of the seed beetle Callosobruchus maculatus (Coleoptera: Bruchidae). These populations had geographically distant (> 2000 km) origins but evolved in a uniform laboratory environment for 120 generations. For each pair of populations (Nigeria x Yemen and Cameroon x Uganda) we estimated the means of five fitness-related characters and a measure of fitness (net reproductive rate R0) in each of the parental populations and 12 types of hybrids (two F1 and two F2 lines and eight backcrosses). Models containing up to nine composite genetic parameters were fitted to the means of the 14 lines. The patterns of line means for all traits in the Nigeria x Yemen cross and for four traits (larval survival, developmental rate, female body weight, and fecundity) in the Cameroon x Uganda cross were best explained by models including additive, dominance, and maternal effects, but excluding epistasis. We did not find any evidence for outbreeding depression for any trait. An epistatic component of divergence was detected for egg hatching success and R0 in the Cameroon x Uganda cross, but its sign was opposite to that expected under outbreeding depression, that is, additive x additive epistasis had a positive effect on the performance of F2 hybrids. All traits except fecundity showed a pattern of heterosis. A large difference of egg-hatching success between the two reciprocal F1 lines in that cross was best explained as fertilization incompatibility between Cameroon females and sperm carrying Uganda genes. The results suggest that these populations have not converged to the same life-history phenotype and genetic architecture, despite 120 generations of uniform natural selection. However, the absence of outbreeding depression implies that they did not evolve toward different adaptive peaks.     

Mate choice, genetic incompatibility, and outbreeding in the ornate dragon lizard, Ctenophorus ornatus

There has been recent interest in the role genetic incompatibility may play in mate or sperm choice. One source of incompatibility may be too similar or disparate genomes. An isolated population of the ornate dragon lizard, Ctenophorus ornatus, was followed over a breeding season and parentage assigned to the offspring using microsatellites. It was found that the adults in the population had an eight per cent chance of mating with a relative. I examined whether C. ornatus mate (or fertilize their eggs) with respect to genetic similarity. There was no difference in a female's relatedness to the male in whose territory she resided and her average relatedness to all other males. Neither was there a difference in the relatedness of the male that sired a female's offspring and the female's average relatedness to all other males. There was no evidence of a cost to mating with a more genetically similar mate, because offspring survival was not influenced by degree of inbreeding or outbreeding. However, females that were more outbred had fewer offspring survive. In this small population there are two possible explanations for the decreased fitness associated with outbreeding. First, the species may have an evolutionary history of inbreeding and thus may be susceptible to outbreeding depression. Second. as fitter individuals produce more offspring, these offspring have an increased probability of breeding with relatives, leading to an indirect relationship between fitness and outbreeding.     

Costs and benefits of admixture between foreign genotypes and local populations in the field

Admixture is the hybridization between populations within one species. It can increase plant fitness and population viability by alleviating inbreeding depression and increasing genetic diversity. However, populations are often adapted to their local environments and admixture with distant populations could break down local adaptation by diluting the locally adapted genomes. Thus, admixed genotypes might be selected against and be outcompeted by locally adapted genotypes in the local environments. To investigate the costs and benefits of admixture, we compared the performance of admixed and within‐population F1 and F2 generations of the European plant Lythrum salicaria in a reciprocal transplant experiment at three European field sites over a 2‐year period. Despite strong differences between site and plant populations for most of the measured traits, including herbivory, we found limited evidence for local adaptation. The effects of admixture depended on experimental site and plant population, and were positive for some traits. Plant growth and fruit production of some populations increased in admixed offspring and this was strongest with larger parental distances. These effects were only detected in two of our three sites. Our results show that, in the absence of local adaptation, admixture may boost plant performance, and that this is particularly apparent in stressful environments. We suggest that admixture between foreign and local genotypes can potentially be considered in nature conservation to restore populations and/or increase population viability, especially in small inbred or maladapted populations.     

Perspective: Evolution of flower color in the desert annual Linanthus parryae: Wright revisited

Linanthus parryae, a diminutive desert annual with white or blue flowers, has been the focus of a long-standing debate among evolutionary biologists. At issue is whether the flower color polymorphism in this species is the product of random genetic drift, as Sewall Wright argued, or of natural selection, as proposed by Carl Epling and his colleagues. Our long-term studies of three polymorphic populations in the Mojave Desert demonstrate that flower color is subject to selection that varies in both time and space in its direction and magnitude. For all sites taken together, blue-flowered plants produced more seeds than white-flowered plants in years of relatively low seed production, whereas white-flowered plants had higher fitness in years of high seed production. Evidence of selection on flower color was found in two of the three study sites. Differences in fitness between the color morphs were sometimes large, with selection coefficients as high as 0.60 in some years. Our longest period of observations was at Pearblossom site 1, where plants reached appreciable densities in seven of the 11 years of study. Here we found significant differences in the seed production of the color morphs in six years, with three years of blue advantage and three years of white advantage. For all sites taken together, total spring precipitation (March and April) was positively correlated with both absolute and relative seed production of the color morphs. At Pearblossom site 1, blue-flowered plants typically had a fitness advantage in years of low spring precipitation, whereas white-flowered plants had a fitness advantage in years of high spring precipitation. This temporal variation in selection may contribute to the maintenance of the flower-color polymorphism at Pearblossom site 1, whereas gene flow from neighboring populations is proposed as the principal factor maintaining the polymorphism at the other study sites. We found no significant differences between the color morphs in pollinator visitation rate or in their carbon isotope ratio, a measure of water-use efficiency. Although the mechanism of selection remains elusive, our results refute Wright's conclusion that the flower color polymorphism in L. parryae is an example of isolation by distance, a key component of his shifting balance theory of evolution.     

Local genetic differentiation for disease resistance in a selfing annual

Electrophoretic analysis of a population of the annual legume Amphicarpaea bracteata revealed that plants in two areas 50 m apart were fixed or nearly fixed for different alleles at eight polymorphic allozyme loci. This multilocus differentiation was highly correlated with variation in disease resistance to the specialist pathogen Synchytrium decipiens : in both laboratory and field experiments, all plants from one area were susceptible, and all plants from the other area were resistant to local pathogen isolates. Analysis of F2 plants from a cross between the two plant biotypes suggested polygenic inheritance of disease resistance, with a minimum of 7–8 loci contributing to the difference among parental lines. The high degree of self-fertilization in A. bracteata , together with spatially restricted seed dispersal, may account for perpetuation of the two divergent plant lineages at this site with little introgression or mixing. Although pathogens could influence the relative frequency of the two host lineages in this habitat, the restricted diversity of local pathogens implies that there may be little selection on plants for outcrossing as a mechanism to reduce pathogen impact.