Divergent Selection Regimes Research Articles

Thermodynamic effects drive countergradient responses in the thermal performance of Littorina saxatilis across latitude

Thermal performance curves (TPCs) provide a powerful framework to assess the evolution of thermal sensitivity in populations exposed to divergent selection regimes across latitude. However, there is a lack of consensus regarding the extent to which physiological adjustments that compensate for latitudinal temperature variation (metabolic cold adaptation; MCA) may alter the shape of TPCs, including potential repercussion on upper thermal limits. To address this, we compared TPCs for cardiac activity in latitudinally-separated populations of the intertidal periwinkle Littorina saxatilis. We applied a non-linear TPC modelling approach to explore how different metrics governing the shape of TPCs varied systematically in response to local adaptation and thermal acclimation. Both critical upper limits, and the temperatures at which cardiac performance was maximised, were higher in the northernmost (cold-adapted) population and displayed a countergradient latitudinal trend which was most pronounced following acclimation to low temperatures. We interpret this response as a knock-on consequence of increased standard metabolic rate in high latitude populations, indicating that physiological compensation associated with MCA may indirectly influence variation in upper thermal limits across latitude. Our study highlights the danger of assuming that variation in any one aspect of the TPC is adaptive without appropriate mechanistic and ecological context.

Punishment controls helper defence against egg predators but not fish predators in cooperatively breeding cichlids

Helping behaviour in some cooperative breeders is apparently maintained by a combination of coercion and reciprocity. In such pay-to-stay systems, alloparental brood care of subordinate group members functions as a service to dominants, which tolerate subordinates based on how much help they provide. Cooperative territory defence is a key task of cooperative breeders, but it is unknown how territory defence by subordinates is socially regulated. Diverse costs and benefits associated with defending the territory against different threats suggest that these defence behaviours may be maintained through divergent selection regimes, and they might be regulated through different social processes. In the cooperatively breeding cichlid fish Neolamprologus pulcher, unrelated subordinates help defend the territory against egg predators even if they do not participate in reproduction and therefore do not suffer direct or indirect fitness costs through predators of eggs. This behaviour has therefore been interpreted as altruistic service to dominants. Subordinates also defend the group territory against predators of juveniles and adults, which might at least partly reflect their own direct fitness interests and could be maintained through mutualistic interactions among group members. Here, we directly compared the regulation of these two types of defence behaviours and tested whether they are enforced by breeders. We prevented subordinates from defending the territory against egg predators or predators of adults and observed whether they received more aggression in response to this treatment. We found that subordinates received more aggression from breeders after withholding defence against egg predators, but not after withholding defence against fish predators. This suggests that territory defence against egg predators by helpers is enforced by breeders and hence subject to negotiations and trading, whereas defence against fish predators is probably based on mutualistic fitness benefits.

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation.

Divergence of genital traits among lineages has the potential to serve as a reproductive isolating barrier when copulation, insemination, and fertilization are inhibited by incompatibilities between female and male genitalia. Despite widespread evidence for genital trait diversity among closely related lineages and coevolution of female and male genitalia within lineages, few studies have investigated genital evolution during the early stages of speciation. We quantified genital variation in replicated population pairs of Poecilia mexicana with ongoing ecological speciation between sulfidic (H2 S containing) and nearby nonsulfidic habitats. These analyses revealed rapid and correlated divergence of female and male genitalia across evolutionarily independent population pairs exposed to divergent selection regimes. Both sexes exhibited convergent evolution of genital traits among populations inhabiting similar habitat types. Our results demonstrate that genital evolution can occur during the early stages of speciation-with-gene-flow, potentially as a result of variation in the intensity of sexual conflict among populations. Our results suggest genitalia may contribute to early stages of divergence and challenge the generality of previously suggested mechanisms of genital evolution in poeciliids.

Consumer-resource interactions along urbanization gradients drive natural selection.

Urbanization is an important component of global change. Urbanization affects species interactions, but the evolutionary implications are rarely studied. We investigate the evolutionary consequences of a common pattern: the loss of high trophic-level species in urban areas. Using a gall-forming fly, Eurosta solidaginis, and its natural enemies that select for opposite gall sizes, we test for patterns of enemy loss, selection, and local adaptation along five urbanization gradients. Eurosta declined in urban areas, as did predation by birds, which preferentially consume gallmakers that induce large galls. These declines were linked to changes in habitat availability, namely reduced forest cover in urban areas. Conversely, a parasitoid that attacks gallmakers that induce small galls was unaffected by urbanization. Changes in patterns of attack by birds and parasitoids resulted in stronger directional selection, but loss of stabilizing selection in urban areas, a pattern which we suggest may be general. Despite divergent selective regimes, gall size did not very systematically with urbanization, suggesting but not conclusively demonstrating that environmental differences, gene flow, or drift, may have prevented the adaptive divergence of phenotypes. We argue that the evolutionary effects of urbanization will have predictable consequences for patterns of species interactions and natural selection.

Range expansion drives the evolution of alternate reproductive strategies in invasive fire ants

Many species are expanding their ranges in response to climate changes or species introductions. Expansion-related selection likely drives the evolution of dispersal and reproductive traits, especially in invasive species introduced into novel habitats. We used an agent-based model to investigate these relationships in the red imported fire ant, Solenopsis invicta, by tracking simulated populations over 25 years. Most colonies of this invasive species produce two types of queens practicing alternate reproductive strategies. Claustral queens found new colonies in vacant habitats, while parasitic queens take over existing colonies whose queens have died. We investigated how relative investment in the two queen types affects population demography, habitat occupancy, and range expansion. We found that parasitic queens extend the ecological lifespan of colonies, thereby increasing a population’s overall habitat occupancy as well as average colony size (number of workers) and territory size. At the same time, investment in parasitic queens slowed the rate of range expansion by diverting investment from claustral queens. Divergent selection regimes caused edge and interior populations to evolve different levels of reproductive investment, such that interior populations invested heavily in parasitic queens whereas those at the edge invested almost entirely in claustral queens. Our results highlight factors shaping ant life histories, including the evolution of social parasitism, and have implications for the response of species to range shifts.

Divergent evolution of life span associated with mitochondrial DNA evolution.

Mitochondria play a key role in ageing. The pursuit of genes that regulate variation in life span and ageing have shown that several nuclear-encoded mitochondrial genes are important. However, the role of mitochondrial encoded genes (mtDNA) is more controversial and our appreciation of the role of mtDNA for the evolution of life span is limited. We use replicated lines of seed beetles that have been artificially selected for long or short life for >190 generations, now showing dramatic phenotypic differences, to test for a possible role of mtDNA in the divergent evolution of ageing and life span. We show that these divergent selection regimes led to the evolution of significantly different mtDNA haplotype frequencies. Selection for a long life and late reproduction generated positive selection for one specific haplotype, which was fixed in most such lines. In contrast, selection for reproduction early in life led to both positive selection as well as negative frequency-dependent selection on two different haplotypes, which were both present in all such lines. Our findings suggest that the evolution of life span was in part mediated by mtDNA, providing support for the emerging general tenet that adaptive evolution of life-history syndromes may involve mtDNA.

The association of feeding behaviour with the resistance and tolerance to parasites in recently diverged sticklebacks.

Divergent natural selection regimes can contribute to adaptive population divergence, but can be sensitive to human-mediated environmental change. Nutrient loading of aquatic ecosystems, for example, might modify selection pressures by altering the abundance and distribution of resources and the prevalence and infectivity of parasites. Here, we used a mesocosm experiment to test for interactive effects of nutrient loading and parasitism on host condition and feeding ecology. Specifically, we investigated whether the common fish parasite Gyrodactylus sp. differentially affected recently diverged lake and stream ecotypes of three-spined stickleback (Gasterosteus aculeatus). We found that the stream ecotype had a higher resistance to Gyrodactylus sp. infections than the lake ecotype, and that both ecotypes experienced a cost of parasitism, indicated by negative relationships between parasite load and both stomach fullness and body condition. Overall, our results suggest that in the early stages of adaptive population divergence of hosts, parasites can affect host resistance, body condition and diet.

Repeated evolution of local adaptation in swimming performance: population-level trade-offs between burst and endurance swimming inBrachyrhaphisfreshwater fish

Specialization is fundamentally important in biology because specialized traits allow species to expand into new environments, in turn promoting population differentiation and speciation. Specialization often results in trade-offs between traits that maximize fitness in one environment but not others. Despite the ubiquity of trade-offs, we know relatively little about how consistently trade-offs evolve between populations when multiple sets of populations experience similarly divergent selective regimes. In the present study, we report a case study on Brachyrhaphis fishes from different predation environments. We evaluate apparent within/between population trade-offs in burst-speed and endurance at two levels of evolutionary diversification: high- and low-predation populations of Brachyrhaphis rhabdophora, and sister species Brachyrhaphis roseni and Brachyrhaphis terrabensis, which occur in high- and low-predation environments, respectively. Populations of Brachyrhaphis experiencing different predation regimes consistently evolved swimming specializations indicative of a trade-off between two swimming forms that are likely highly adaptive in the environment in which they occur. We show that populations have become similarly locally adapted at both levels of diversification, suggesting that swimming specialization has evolved rather rapidly and persisted post-speciation. Our findings provide valuable insight into how local adaptation evolves at different stages of evolutionary divergence.

Can divergent selection save the rare Senecio hercynicus from genetic swamping by its spreading congener S. ovatus (Compositae, Senecioneae)?

Hybridisation leading to genetic swamping of a rare species by its more common congener is considered to become an issue of growing importance in conservation biology due to the fact that an increasing human impact on natural habitats and changes in climatic conditions will lead to higher frequencies of hybrid formation by shifting distributions and/or phenologies. In order to judge the future trajectories of hybridising plant species, which could eventually lead to the loss of taxonomic biodiversity, it is necessary to discern scenarios that lead to a complete merging of two species from those where hybridisation is an intermediary stage towards the establishment of reproductively isolated entities. We present a population-genomic approach that may allow discriminating between these two scenarios by estimating the strength of divergent selection regimes in hybrid swarms along ecological gradients. Using AFLP fingerprinting, 196 individuals from 11 populations of Senecio hercynicus and S. ovatus along an elevational transect (750–1300m) in the Bavarian Forest National Park were genotyped for 634 anonymous loci. Based on Bayesian cluster algorithms, all populations were identified as being hybrid swarms with different admixture proportions of both parental genotypes, indicating the intense introgressive hybridisation realised in this hybrid zone. Searching for loci under selection by using either FST-based or logistic regression model-based techniques resulted in the identification of only few AFLP markers under selection, which showed a significant correlation with some climatic variables along the transect. The simultaneous finding, however, that species-specific markers were not among these selected markers support the interpretation that there is no climatically mediated divergent selection or reinforcement process going on that could (re-)establish genetically isolated (biological) species.

Ontogenetic shifts in phenotype-environment associations in Nile perch,Lates niloticus(Perciformes: Latidae) from Lake Nabugabo, Uganda

Habitat-associated trait divergence may vary across ontogeny if there are strong size-related shifts in selection pressures. We quantified patterns of phenotypic divergence in Nile perch (Lates niloticus) from ecologically distinct wetland edge and forest edge habitats in Lake Nabugabo, Uganda, and we compared patterns of divergence across three size classes to determine whether trends are consistent through Nile perch ontogeny. We predicted that inter-habitat variation in biotic (e.g. vegetation structure) and abiotic (e.g. dissolved oxygen concentration) variables may create divergent selective regimes. We compared body morphology using geometric morphometrics and found substantial differences between habitats, although not all trends were consistent across size classes. The most striking aspects of divergence in small Nile perch were in mouth orientation, head size, and development of the caudal region. Medium-sized Nile perch also showed differences in mouth orientation. Differences in large individuals were related to eye size and orientation, as well as caudal length. The observed patterns of divergence are consistent with functional morphological predictions for fish across divergent trophic regimes, high and low predation environments, and complex and simple habitats. Although this suggests adaptive divergence, the source of phenotypic variation is unknown and may reflect phenotypic plasticity and/or genetic differences. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 449–465.

Adaptive plasticity and genetic divergence in feeding efficiency during parallel adaptive radiation of whitefish (Coregonusspp.)

Parallel phenotypic divergence in replicated adaptive radiations could either result from parallel genetic divergence in response to similar divergent selection regimes or from equivalent phenotypically plastic response to the repeated occurrence of contrasting environments. In post-glacial fish, replicated divergence in phenotypes along the benthic-limnetic habitat axis is commonly observed. Here, we use two benthic-limnetic species pairs of whitefish from two Swiss lakes, raised in a common garden design, with reciprocal food treatments in one species pair, to experimentally measure whether feeding efficiency on benthic prey has a genetic basis or whether it underlies phenotypic plasticity (or both). To do so, we offered experimental fish mosquito larvae, partially burried in sand, and measured multiple feeding efficiency variables. Our results reveal both, genetic divergence as well as phenotypically plastic divergence in feeding efficiency, with the phenotypically benthic species raised on benthic food being the most efficient forager on benthic prey. This indicates that both, divergent natural selection on genetically heritable traits and adaptive phenotypic plasticity, are likely important mechanisms driving phenotypic divergence in adaptive radiation.

Genomic signatures of relaxed disruptive selection associated with speciation reversal in whitefish

BackgroundSpeciation reversal: the erosion of species differentiation via an increase in introgressive hybridization due to the weakening of previously divergent selection regimes, is thought to be an important, yet poorly understood, driver of biodiversity loss. Our study system, the Alpine whitefish (Coregonus spp.) species complex is a classic example of a recent postglacial adaptive radiation: forming an array of endemic lake flocks, with the independent origination of similar ecotypes among flocks. However, many of the lakes of the Alpine radiation have been seriously impacted by anthropogenic nutrient enrichment, resulting in a collapse in neutral genetic and phenotypic differentiation within the most polluted lakes. Here we investigate the effects of eutrophication on the selective forces that have shaped this radiation, using population genomics. We studied eight sympatric species assemblages belonging to five independent parallel adaptive radiations, and one species pair in secondary contact. We used AFLP markers, and applied FST outlier (BayeScan, Dfdist) and logistic regression analyses (MatSAM), to identify candidate regions for disruptive selection in the genome and their associations with adaptive traits within each lake flock. The number of outlier and adaptive trait associated loci identified per lake were then regressed against two variables (historical phosphorus concentration and contemporary oxygen concentration) representing the strength of eutrophication.ResultsWhilst we identify disruptive selection candidate regions in all lake flocks, we find similar trends, across analysis methods, towards fewer disruptive selection candidate regions and fewer adaptive trait/candidate loci associations in the more polluted lakes.ConclusionsWeakened disruptive selection and a concomitant breakdown in reproductive isolating mechanisms in more polluted lakes has lead to increased gene flow between coexisting Alpine whitefish species. We hypothesize that the resulting higher rates of interspecific recombination reduce either the number or extent of genomic islands of divergence surrounding loci evolving under disruptive natural selection. This produces the negative trend seen in the number of selection candidate loci recovered during genome scans of whitefish species flocks, with increasing levels of anthropogenic eutrophication: as the likelihood decreases that AFLP restriction sites will fall within regions of heightened genomic divergence and therefore be classified as FST outlier loci. This study explores for the first time the potential effects of human-mediated relaxation of disruptive selection on heterogeneous genomic divergence between coexisting species.

Disruption of gene expression in hybrids of the fire ants Solenopsis invicta and Solenopsis richteri

Transcriptome analysis is a powerful tool for unveiling the distribution and magnitude of genetic incompatibilities between hybridizing taxa. The nature of such incompatibilities is closely associated with the evolutionary histories of the parental species and may differ across tissues and between the sexes. In eusocial insects, the presence of castes that experience divergent selection regimes may result in additional distinct patterns of caste-specific hybrid incompatibilities. We analysed levels of expression of >14,000 genes in two life stages of each caste in the fire ants Solenopsis invicta and Solenopsis richteri and in their hybrids. We found strong contributions of both developmental stage and caste to gene expression patterns. In contrast, variability in expression was only weakly associated with taxonomic identity, with hybrid scores falling between those of the two parental species. Hybrid incompatibilities were surprisingly modest, with only 32 genes being mis-expressed, indicating low levels of disruption in gene regulation in hybrids; males and workers each mis-expressed at least seven times as many genes as queens. Interestingly, homologues of many of the mis-expressed genes have been implicated in behavioural variation in Drosophila melanogaster. General expression profiles of hybrids consistently were more similar to those of S. richteri than S. invicta, presumably because S. richteri trans-regulatory elements tend to be dominant and/or because there is an overall bias in the genetic composition of the hybrids towards S. richteri. Altogether, our results suggest that selection acting on each caste may contribute differently to interspecific divergence and speciation in this group of ants.

Detecting selection on morphological traits in social insect castes: the case of the social wasp Vespula maculifrons

Highly social insects dominate terrestrial ecosystems because society members belong to discrete castes that undertake distinct tasks. The distinct functional roles of members of different castes may lead to divergent selective regimes, which may ultimately lead to morphological specialization and differentiation of the castes. This study used morphological and genetic analyses to identify traits that experienced caste-specific selection in the social wasp Vespula maculifrons (Buysson, 1905). Traits putatively under selection were identified based on their degree of caste dimorphism, levels of variability, strength of correlations with other traits, and patterns of allometric scaling. Analyses of trait characteristics suggested that queen thorax length, thorax width, and possibly mass, have experienced queen-specific selection. Additionally, trait dimorphism and intercaste phenotypic correlation values were negatively correlated, as expected if some morphological traits were subject to selection, leading to alternate phenotypic optima in the two castes. Overall, our analyses demonstrate how techniques used to identify selection between dimorphic groups can be applied to social species with distinct castes. In addition, our analyses suggest the operation of selection may be stronger in reproductive than in non-reproductive castes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 93–102. ADDITIONAL KEYWORDS: allometry – dimorphism – genetic architecture – genetic correlation – Hymenoptera – morphology – social insect – yellowjacket.

Intrabreed Stratification Related to Divergent Selection Regimes in Purebred Dogs May Affect the Interpretation of Genetic Association Studies

Until recently, canine genetic research has not focused on population structure within breeds, which may confound the results of case―control studies by introducing spurious correlations between phenotype and genotype that reflect population history. Intrabreed structure may exist when geographical origin or divergent selection regimes influence the choices of potential mates for breeding dogs. We present evidence for intrabreed stratification from a genome-wide marker survey in a sample of unrelated dogs. We genotyped 76 Border Collies, 49 Australian Shepherds, 17 German Shepherd Dogs, and 17 Portuguese Water Dogs for our primary analyses using Affymetrix Canine v2.0 single-nucleotide polymorphism (SNP) arrays. Subsets of autosomal markers were examined using clustering algorithms to facilitate assignment of individuals to populations and estimation of the number of populations represented in the sample. SNPs passing stringent quality control filters were employed for explicitly phylogenetic analyses reconstructing relationships between individuals using maximum parsimony and Bayesian methods. We used simulation studies to explore the possible effects of intrabreed stratification on genome-wide association studies. These analyses demonstrate significant stratification in at least one of our primary breeds of interest, the Border Collie. Demographic and pedigree data suggest that this population substructure may result from geographic isolation or divergent selection regimes practiced by breeders with different breeding program goals. Simulation studies indicate that such stratification could result in false discovery rates significant enough to confound genome-wide association analyses. Intrabreed stratification should be accounted for when designing and interpreting the results of case― control association studies using purebred dogs.

Population genetic structure across dissolved oxygen regimes in an African cichlid fish

Ecological isolation is a process whereby gene flow between selective environments is reduced due to selection against maladapted dispersers, migrant alleles, or hybrids. Although ecological isolation has been documented in several systems, gene flow can often be high among selective regimes, and more studies are thus needed to better understand the conditions under which ecological gradients or divergent selective regimes should influence population structure. We test for ecological isolation in a system in which high plasticity occurs with respect to traits that are adaptive in alternate forms under different environmental conditions. Pseudocrenilabrus multicolor victoriae is a widespread haplochromine cichlid fish in East Africa that exploits both normoxic (normal oxygen) rivers/lakes and hypoxic (low oxygen) swamps. Here, we examine population structure, using mitochondrial DNA and microsatellites, to determine if genetic divergence is significantly increased between dissolved oxygen regimes relative to within them, while controlling for geographical structure. Our results indicate that geographical separation influences population structure, while no effects of divergent selection with respect to oxygen regimes were detected. Specifically, we document (i) genetic clustering according to geographical region, but no clustering according to oxygen regime; (ii) higher genetic variation among than within regions, but no effect of oxygen regime on genetic variation; (iii) isolation by distance within one region; and (iv) decreasing genetic variability with increasing geographical distance from Lake Victoria. We speculate that plasticity may be facilitating gene flow between oxygen regimes in this system.

Linked selected and neutral loci in heterogeneous environments.

We analyze a system of ordinary differential equations modeling haplotype frequencies at a physically linked pair of loci, one selected and one neutral, in a population consisting of two demes with divergent selection regimes. The system is singularly perturbed, with the migration rate m between the demes serving as a small parameter. We use geometric singular perturbation theory to show that when m is sufficiently small, each solution not initially fixed for the same selected allele in both demes approaches one of a 1-dimensional continuum of equilibria. We then obtain asymptotic expansions of the solutions and show their validity on arbitrarily long finite time intervals. From these expansions we obtain formulas for the transient dynamics of F(ST) (a measure of population structure) at both loci, as well as for the rate of genotyping error if the allelic state at the selected locus is inferred from that at the neutral (marker) locus. We examine two cases in detail, one modeling two populations in secondary contact after a period of evolution in allopatry, and the other modeling the origination and spread of a resistance allele.

A Thirty-Year Study of Phenotypic and Genetic Variation of Blue Tits in Mediterranean Habitat Mosaics

Abstract In recent years, the study of phenotypic and genetic variation has been enhanced by combining genetic, physiological, demographic, and behavioral components of life histories. Using these new approaches, we address the problem of adaptation to environmental heterogeneity by examining in detail the variation of several fitness-related traits in a small passerine bird, the blue tit, which has been extensively studied in habitat mosaics of the Mediterranean region. The response of blue tits to spatial habitat heterogeneity depends on their range of dispersal relative to the size of habitat patches. Dispersal over short distances leads to local specialization, whereas dispersal over long distances leads to phenotypic plasticity. Gene flow between habitats of different quality may produce local maladaptation and a source–sink population structure. However, when habitat-specific divergent selection regimes are strong enough to oppose the effects of gene flow, local adaptation may arise on a scale that ...

Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon.

Colonization of new environments should promote rapid speciation as a by-product of adaptation to divergent selective regimes. Although this process of ecological speciation is known to have occurred over millennia or centuries, nothing is known about how quickly reproductive isolation actually evolves when new environments are first colonized. Using DNA microsatellites, population-specific natural tags, and phenotypic variation, we tested for reproductive isolation between two adjacent salmon populations of a common ancestry that colonized divergent reproductive environments (a river and a lake beach). We found evidence for the evolution of reproductive isolation after fewer than 13 generations.

Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika

The current phylogenetic hypothesis for the endemic Lake Tanganyika cichlid fishes of the tribe Eretmodini is based solely on morphology and suggests that more complex trophic morphologies derived only once from a less specialized ancestral condition. A molecular phylogeny of eretmodine cichlids based on partial mitochondrial DNA cytochrome b and control-region sequences was used to reconstruct the evolutionary sequence of trophic adaptations and to test alternative models of morphological divergence. The six mitochondrial lineages found disagree with the current taxonomy and the morphology-based phylogeny. Mitochondrial lineages with similar trophic morphologies are not grouped monophyletically but are typically more closely related to lineages with different trophic phenotypes currently assigned to other genera. Our results indicate multiple independent origins of similar trophic specializations in these cichlids. A pattern of repeated divergent morphological evolution becomes apparent when the phylogeography of the mitochondrial haplotypes is analyzed in the context of the geological and paleoclimatological history of Lake Tanganyika. In more than one instance within Lake Tanganyika, similar morphological divergence of dentitional traits occurred in sympatric species pairs. Possibly, resource-based divergent selective regimes led to resource partitioning and brought about similar trophic morphologies independently and repeatedly.