Genomic regions with a history of divergent selection affect fitness of hybrids between two butterfly species

Speciation is the process by which reproductively isolated lineages arise, and is one of the fundamental means by which the diversity of life increases. Whereas numerous studies have documented an association between ecological divergence and reproductive isolation, relatively little is known about the role of natural selection in genome divergence during the process of speciation. Here, we use genome-wide DNA sequences and Bayesian models to test the hypothesis that loci under divergent selection between two butterfly species (Lycaeides idas and L. melissa) also affect fitness in an admixed population. Locus-specific measures of genetic differentiation between L. idas and L. melissa and genomic introgression in hybrids varied across the genome. The most differentiated genetic regions were characterized by elevated L. idas ancestry in the admixed population, which occurs in L. idas-like habitat, consistent with the hypothesis that local adaptation contributes to speciation. Moreover, locus-specific measures of genetic differentiation (a metric of divergent selection) were positively associated with extreme genomic introgression (a metric of hybrid fitness). Interestingly, concordance of differentiation and introgression was only partial. We discuss multiple, complementary explanations for this partial concordance.     

The uncertainty of "fitness:" what prevents understanding of the role of genetic exchange

The evolutionary development of highly organized species is attained through an increase in average survival of individuals, whereas the evolution of primitive species involves only an increase in fecundity (Zavadsky, 1958, 1961). However, in population genetics, survival (or ecological resistance) and fecundity are regarded as components of a single character, fitness. Employment of the notion of fitness, which lacks a strict definition, hinders understanding of the mechanism of progressive evolution as the process that enhances ecological resistance of organisms. The notion of fitness also exacerbates understanding the role of genetic exchange, since the primary advantage of genetic recombination and sexual reproduction apparently is producing of progeny with high ecological resistance rather than with high genetic diversity as such. Thus, the regular genetic exchange ensures restoration of the level of ecological resistance characteristic for the species, and on the macroevolutionary scale leads to the formation of new genomes and new species with high ecological resistance.     

The Uncertainty of “Fitness”: What Prevents Understanding of the Role of Genetic Exchange

The evolutionary development of highly organized species is attained through an increase in average survival of individuals, whereas the evolution of primitive species involves only an increase in fecundity (Zavadsky, 1968). However, in population genetics, survival (or ecological resistance) and fecundity are regarded as components of a single character, fitness. Employment of the notion of fitness, which lacks a strict definition, hinders understanding of the mechanism of progressive evolution as the process that enhances ecological resistance of organisms. The notion of fitness also hinders understanding the role of genetic exchange, since the primary advantage of genetic recombination and sexual reproduction apparently is producing of progeny with high ecological resistance rather than with high genetic diversity as such. Thus, the regular genetic exchange ensures restoration of the level of ecological resistance characteristic for the species, and on the macroevolutionary scale leads to the formation of new genomes and new species with high ecological resistance.     

Environment-specific heterozygote deficiency and developmental instability in hybrid Mytilus

The multiple discrete hybrid zones that characterize Mytilus blue mussels allow a novel, non-manipulative, examination of the selective pressures that create and maintain species. If endogenous genetic incompatibility is solely responsible for post-zygotic isolation, then individuals of a specified hybrid genotype are expected to show similar average fitness across environments. However, if hybrid fitness differs across environments, then exogenous selection is implicated, either via ecological selection or environment-specific expression of intrinsic genetic incompatibilities. Correspondence between developmental instability of hybrids and heterozygote deficiency, estimated in two M. trossulus×M. galloprovincialis hybrid zones on the coast of North America, indicates that environment-dependent selection against hybrids may contribute to reproductive isolation among Pacific Mytilus species.     

Defence systems and horizontal gene transfer in bacteria

Horizontal gene transfer (HGT) is a fundamental process in prokaryotic evolution, contributing significantly to diversification and adaptation. HGT is typically facilitated by mobile genetic elements (MGEs), such as conjugative plasmids and phages, which often impose fitness costs on their hosts. However, a considerable number of bacterial genes are involved in defence mechanisms that limit the propagation of MGEs, suggesting they may actively restrict HGT. In our study, we investigated whether defence systems limit HGT by examining the relationship between the HGT rate and the presence of 73 defence systems across 12 bacterial species. We discovered that only six defence systems, three of which were different CRISPR-Cas subtypes, were associated with a reduced gene gain rate at the species evolution scale. Hosts of these defence systems tend to have a smaller pangenome size and fewer phage-related genes compared to genomes without these systems. This suggests that these defence mechanisms inhibit HGT by limiting prophage integration. We hypothesize that the restriction of HGT by defence systems is species-specific and depends on various ecological and genetic factors, including the burden of MGEs and the fitness effect of HGT in bacterial populations.     

Testing for local adaptation and evolutionary potential along altitudinal gradients in rainforest Drosophila: beyond laboratory estimates

Predicting how species will respond to the rapid climatic changes predicted this century is an urgent task. Species distribution models (SDMs) use the current relationship between environmental variation and species’ abundances to predict the effect of future environmental change on their distributions. However, two common assumptions of SDMs are likely to be violated in many cases: (i) that the relationship of environment with abundance or fitness is constant throughout a species’ range and will remain so in future and (ii) that abiotic factors (e.g. temperature, humidity) determine species’ distributions. We test these assumptions by relating field abundance of the rainforest fruit fly Drosophila birchii to ecological change across gradients that include its low and high altitudinal limits. We then test how such ecological variation affects the fitness of 35 D. birchii families transplanted in 591 cages to sites along two altitudinal gradients, to determine whether genetic variation in fitness responses could facilitate future adaptation to environmental change. Overall, field abundance was highest at cooler, high‐altitude sites, and declined towards warmer, low‐altitude sites. By contrast, cage fitness (productivity) increased towards warmer, lower‐altitude sites, suggesting that biotic interactions (absent from cages) drive ecological limits at warmer margins. In addition, the relationship between environmental variation and abundance varied significantly among gradients, indicating divergence in ecological niche across the species’ range. However, there was no evidence for local adaptation within gradients, despite greater productivity of high‐altitude than low‐altitude populations when families were reared under laboratory conditions. Families also responded similarly to transplantation along gradients, providing no evidence for fitness trade‐offs that would favour local adaptation. These findings highlight the importance of (i) measuring genetic variation in key traits under ecologically relevant conditions, and (ii) considering the effect of biotic interactions when predicting species’ responses to environmental change.     

Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations

Theory predicts that reproductive isolation may be due to intrinsic genetic incompatibilities or extrinsic ecological factors. Therefore, an understanding of the genetic basis of isolation may require analyses of evolutionary processes in situ to include environmental factors. Here we study genetic isolation between populations of sculpins ( Cottus ) at 168 microsatellites. Genomic clines were fit using 480 individuals sampled across independent natural hybrid zones that have formed between one invading species and two separate populations of a resident species. Our analysis tests for deviations from neutral patterns of introgression at individual loci based on expectations given genome-wide admixture. Roughly 51% of the loci analysed displayed significant deviations. An overall deficit of interspecific heterozygotes in 26% and 21% of the loci suggests that widespread underdominance drives genomic isolation. At the same time, selection promotes introgression of almost 30% of the markers, which implies that hybridization may increase the fitness of admixed individuals. Cases of overdominance or epistatic interactions were relatively rare. Despite the similarity of the two hybrid zones in their overall genomic composition, patterns observed at individual loci show little correlation between zones and many fit different genotypic models of fitness. At this point, it remains difficult to determine whether these results are due to differences in external selection pressures or cryptic genetic differentiation of distinct parental populations. In the future, data from mapped genetic markers and on variation of ecological factors will provide additional insights into the contribution of these factors to variation in the evolutionary consequences of hybridization.     

Structural equation modelling analysis of evolutionary and ecological patterns in Australian Banksia

Evolutionary history of species, their geographic ranges, ecological ranges, genetic diversity, and resistance to pathogen infection, have been viewed as being mutually linked through a complex network of interactions. Previous studies have described simple correlations between pairs of these factors, while rarely separated the direct effects among multiple interacting factors. This study was to separate the effect of multiple interacting factors, to reveal the strength of the interactions among these factors, and to explore the mechanisms underlying the ecological and evolutionary processes shaping the geographic range, genetic diversity and fitness of species. I assembled comparative data on evolutionary history, geographic range, ecological range, genetic diversity, and resistance to pathogen infection for thirteen Banksia species from Australia. I used structural equation modelling to test multivariate hypotheses involving evolutionary history, geographic range, genetic diversity and fitness. Key results are: (1) Species with longer evolutionary times tend to occupy larger geographic ranges; (2) higher genetic diversity is directly associated with longer flowering duration in Banksia; and (3) species with higher genotypic diversity have higher level of resistance to infection caused by the pathogen Phytophthora cinnamomi, whereas heterozygosity has the opposite relationship with capacity of resistance to the infections caused by this pathogen. These results revealed a mutually linked and complex network of interactions among gene, species, environment and pathogen in evolutionary and ecological scales. These findings also have great practical significance and help to provide preemptive management options in pathogen control.     

Genomic compatibility occurs over a wide range of parental genetic similarity in an outcrossing plant

The theory of inbreeding and outbreeding suggests that there is a hump-shaped relationship between the genetic similarity of sexually reproducing parents and the performance of their offspring. Inbreeding depression occurs when genetic similarity is high, whereas hybrid breakdown is expected when genetic similarity is low. Between these extremes, the effect of genetic similarity on fitness is unclear. We studied the shape of this relationship by crossing 65 target genotypes of the clonal, self-incompatible Ranunculus reptans with partner genotypes spanning a broad scale of genetic similarity, ranging from crosses within populations to between-population crosses and hybridisation with a closely related species. Offspring were raised in outdoor tubs. Results revealed a quadratic relationship between parental genetic distance and offspring performance, with the clonal component of fitness more strongly hump-shaped than the sexual component. Optimal genetic similarity encompassed a broad range of within-population and between-population crosses. This pattern of genomic compatibility has important implications for the evolution of mating systems and mate choice.     

Maladaptive Habitat Use of a North American Woodpecker in Population Decline

Rapid anthropogenic habitat changes can lead to non‐ideal habitat use by animals, often resulting in lower fitness and population declines. An extreme case of use and fitness mismatch is an ecological trap where habitat quality cues are disjointed from the true quality of the habitat. Species primarily associated with anthropogenically altered habitat, such as red‐headed woodpeckers (Melanerpes erythrocephalus), may be especially vulnerable to use and fitness mismatch as they encounter novel environmental challenges. We investigated multi‐scale habitat use and nesting success of red‐headed woodpeckers to assess their vulnerability to mismatches between use and fitness as a result of non‐ideal habitat use across multiple scales. We found that habitat characteristics that promote feeding potential such as canopy openness and greater dead limb length appeared paramount and were consistent in use across several spatial scales although reproductive fitness suffered. This contrasts with the assumption that habitat use by nesting birds should instead favor predation avoidance at smaller scales to improve reproductive fitness and suggests that maladaptive, food‐based habitat use by red‐headed woodpeckers in southern Ontario may result in ecological traps for the species. Whether due to poor habitat choices or costly ones in favor of feeding potential, it is vital to consider this behavior in conservation and management plans for this and similar species. We suggest multi‐scale habitat use studies that consider fitness outcomes are critical for species‐at‐risk in human‐modified landscapes.     

Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks

Experimental work has provided evidence for extrinsic post-zygotic isolation, a phenomenon unique to ecological speciation. The role that ecological components to reduced hybrid fitness play in promoting speciation and maintaining species integrity in the wild, however, is not as well understood. We addressed this problem by testing for selection against naturally occurring hybrids in two sympatric species pairs of benthic and limnetic threespine sticklebacks (Gasterosteus aculeatus). If post-zygotic isolation is a significant reproductive barrier, the relative frequency of hybrids within a population should decline significantly across the life-cycle. Such a trend in a natural population would give independent support to experimental evidence for extrinsic, rather than intrinsic, post-zygotic isolation in this system. Indeed, tracing mean individual hybridity (genetic intermediateness) across three life-history stages spanning four generations revealed just such a decline. This provides compelling evidence that extrinsic selection plays an important role in maintaining species divergence and supports a role for ecological speciation in sticklebacks.     

A genetic interpretation of ecologically dependent isolation

Hybrids may suffer a reduced fitness both because they fall between ecological niches (ecologically dependent isolation) and as a result of intrinsic genetic incompatibilities between the parental genomes (ecologically independent isolation). Whereas genetic incompatibilities are common to all theories of speciation, ecologically dependent isolation is a unique prediction of the ecological model of speciation. This prediction can be tested using reciprocal transplants in which the fitness of various genotypes is evaluated in both parental habitats. Here we expand a quantitative genetic model of Lynch (1991) to include two parental environments. We ask whether a sufficient experimental design exists for detecting ecologically dependent isolation. Analysis of the model reveals that by using both backcrosses in both parental environments, environment-specific additive genetic effects can be estimated while correcting for any intrinsic genetic isolation. Environment-specific dominance effects can also be estimated by including the F1 and F2 in the reciprocal transplant. In contrast, a reciprocal transplant comparing only F1s or F2s to the parental species cannot separate ecologically dependent from intrinsic genetic isolation. Thus, a reduced fitness of F1 or F2 hybrids relative to the parental species is not sufficient to demonstrate ecological speciation. The model highlights the importance of determining the contribution of genetic and ecological mechanisms to hybrid fitness if inferences concerning speciation mechanisms are to be made.     

A meta-analysis of the relation between mating system,growth form and genotypic diversity in clonal plant species

Next to its well-described ecological advantages, clonal growth in plants may incur fitness costs, which are associated with the effects of typically large clonal individuals on the patterns of pollen dispersal. These fitness costs include increased selfing and inbreeding depression in self-compatible species, and reduced mate availability in self-incompatible species. Although fitness costs may affect mating system evolution, there is currently no strong evidence available that either self-compatibility or self-incompatibility is associated with clonality. One reason for this may be the variety in growth forms (from guerrilla to phalanx habits) within clonal species, and the fact that growth form may strongly affect mating patterns. We present the results of a formal meta-analysis of 72 published studies, aiming at reporting genotypic diversities across studies and at relating mating system with clonal growth form and genotypic diversity. We found lower genotypic diversities in clonal self-incompatible species compared to self-compatible species, suggesting that mate availability may indeed be reduced in clonal self- incompatible species. We also cannot confirm that mating system is associated with clonal growth form.     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.     

Genetic and morphological divergence along the littoral–pelagic axis in two common and sympatric fishes: perch,Perca fluviatilis (Percidae) and roach,Rutilus rutilus (Cyprinidae)

Individuals are constantly in competition with one another and, on both ecological and evolutionary timescales, processes act to reduce this competition and promote the gain of fitness advantages via diversification. Here we have investigated the genetic (AFLP) and morphological (geometric morphometrics) aspects of the littoral–pelagic axis, a commonly observed resource polymorphism in freshwater fishes of postglacial lakes. We found a large degree of variation in the genetic and morphological divergence between littoral and pelagic perch and roach across Swedish lakes. Although there was evidence of assortative mating (elevated kinship values) in both species, we could not find any significant coupling of morphology and genetic divergence. Instead, there was evidence that the extent of resource polymorphism may be largely caused by phenotypic plasticity. These results suggest that assortative mating, which can lead to genetically determined adaptive divergence, does occur in these species, particularly perch, but not according to genetically fixed morphological traits. The behavioural mechanisms facilitating associative mating need to be investigated to explore the interaction between phenotypic plasticity and adaptive genetic divergence and their roles in diversification. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 929–940.     

Parental genetic similarity and offspring performance in blue tits in relation to brood size manipulation

In birds, as in many other taxa, higher genetic similarity of mates has long been known to reduce offspring fitness. To date, the majority of avian studies have focused on examination whether the genetic similarity of social mates predicts hatching success. Yet, increased genetic similarity of mates may also reduce offspring fitness during later life stages, including the nestling period and beyond. Here, we investigated whether parental genetic similarity influences offspring performance using data from free‐living blue tits (Cyanistes caeruleus) collected across three breeding seasons. Additionally, we tested whether brood size manipulation affects the magnitude and direction of the relationship between genetic similarity of mates and offspring performance. Sixteen microsatellite markers were used to measure genetic similarity between biological parents. We found that the genetic similarity of parents negatively affects offspring immune response and this effect was independent of the experimental brood size manipulation.     

A genetic similarity rule determines arthropod community structure

We define a genetic similarity rule that predicts how genetic variation in a dominant plant affects the structure of an arthropod community. This rule applies to hybridizing cottonwood species where plant genetic variation determines plant-animal interactions and structures a dependent community of leaf-modifying arthropods. Because the associated arthropod community is expected to respond to important plant traits, we also tested whether plant chemical composition is one potential intermediate link between plant genes and arthropod community composition. Two lines of evidence support our genetic similarity rule. First, in a common garden experiment we found that trees with similar genetic compositions had similar chemical compositions and similar arthropod compositions. Second, in a wild population, we found a similar relationship between genetic similarity in cottonwoods and the dependent arthropod community. Field data demonstrate that the relationship between genes and arthropods was also significant when the hybrids were analysed alone, i.e. the pattern is not dependent upon the inclusion of both parental species. Because plant-animal interactions and natural hybridization are common to diverse plant taxa, we suggest that a genetic similarity rule is potentially applicable, and may be extended, to other systems and ecological processes. For example, plants with similar genetic compositions may exhibit similar litter decomposition rates. A corollary to this genetic similarity rule predicts that in systems with low plant genetic variability, the environment will be a stronger factor structuring the dependent community. Our findings argue that the genetic composition of a dominant plant can structure higher order ecological processes, thus placing community and ecosystem ecology within a genetic and evolutionary framework. A genetic similarity rule also has important conservation implications because the loss of genetic diversity in one species, especially dominant or keystone species that define many communities, may cascade to negatively affect the rest of the dependent community.     

Phenotypic similarity and the evolutionary significance of countergradient variation

Countergradient variation is a geographical pattern of genotypes (with respect to environments) in which genetic influences on a trait oppose environmental influences, thereby minimizing phenotypic change along the gradient. Phenotypic similarity across changing environments ought to be of intense interest because it belies considerable genotypic change. When it occurs in characters that are positively associated with fitness, countergradient variation conflicts with the hypothesis that local adaptation to one environment trades off against performance in another environment. Cases of countergradient variation therefore offer unique insight into the mechanisms that produce and maintain phenotypic similarity and/or differences along environmental gradients.     

Diversification across a heterogeneous landscape

Adaptation to contrasting environments across a heterogeneous landscape favors the formation of ecotypes by promoting ecological divergence. Patterns of fitness variation in the field can show whether natural selection drives local adaptation and ecotype formation. However, to demonstrate a link between ecological divergence and speciation, local adaptation must have consequences for reproductive isolation. Using contrasting ecotypes of an Australian wildflower, Senecio lautus in common garden experiments, hybridization experiments, and reciprocal transplants, we assessed how the environment shapes patterns of adaptation and the consequences of adaptive divergence for reproductive isolation. Local adaptation was strong between ecotypes, but weaker between populations of the same ecotype. F1 hybrids exhibited heterosis, but crosses involving one native parent performed better than those with two foreign parents. In a common garden experiment, F2 hybrids exhibited reduced fitness compared to parentals and F1 hybrids, suggesting that few genetic incompatibilities have accumulated between populations adapted to contrasting environments. Our results show how ecological differences across the landscape have created complex patterns of local adaptation and reproductive isolation, suggesting that divergent natural selection has played a fundamental role in the early stages of species diversification.     

Inbreeding and interbreeding in Darwin's finches

Studies of inbreeding and interspecific hybridization are generally pursued separately with different metrics. There is a need to integrate them because they have the common goal of seeking an understanding of the genetic and ecological basis of fitness variation in populations. We use mean expected heterozygosity as an axis of variation on which to compare the fitness of inbreeding and hybridizing Darwin's finches (Geospiza scandens and G. fortis) relative to the fitness of matched outbred controls. We find that relative fitness of inbred finches is less than one in the 1991 cohorts of both species. Inbreeding depression is stronger in the species (G. scandens) with the lower genetically effective population size. Relative fitness of hybrids (backcrosses) in the same cohort of G. scandens is greater than one. Evidence of heterosis in G. fortis is mixed. Thus the two interbreeding species displayed somewhat different fitness patterns under the same set of environmental conditions. Hybridization may enhance fitness to different degrees by counteracting the effects of inbreeding depression, by other additive and nonadditive genetic effects, and by producing phenotypes well suited to exploit particular ecological conditions.