Geographic Mosaic Of Selection Research Articles

A small‐tiled geographic mosaic of coevolution between Eurosta solidaginis and its natural enemies and host plant

AbstractWe identified a geographic mosaic of Eurosta solidaginis fly traits produced by coevolution of the stem gall‐forming fly with both its natural enemies and its host plants at small geographic scales in the presence of gene flow. These tritrophic interactions between the fly with its natural enemies and with its host‐plant Solidago altissima produced what has been termed a small‐tiled geographic mosaic of coevolution. Selection on gall diameter and length varies between prairie and forest habitats due to differences in host plants and natural‐enemy communities. At the prairie–forest ecotone where prairie and forest habitats are intermixed, we found that geographic selection mosaics on gall diameter and length varied on a scale of a few kilometers. Gall diameter variation among sites correlated with selection on gall diameters, indicating local adaptation. In contrast, gall lengths did not correlate with selection, indicating that gene flow may have prevented local adaptation of this trait. Eastern (forest) and western (prairie) subspecies of E. solidaginis have been proposed based on fly wing patterns, and these had intermediate forms in the ecotone indicating gene flow between these subspecies. Variation in wing patterns correlated with gall diameter, indicating that gene flow between prairie and forest fly populations may influence the distribution of gall traits. The ratio of forest to prairie vegetation increases with latitude, but there was no indication of latitudinal clines in gall or wing traits. Our results indicate that selection for differentiation in coevolved traits is strong enough to overcome gene flow in small tiles of habitat. The result is that ecological forces produce a dynamic mosaic of genetically differentiated locally adapted populations. It also indicates that prairie and forest host races of E. solidaginis form a mosaic hybrid zone in this region.

Genomics of sorghum local adaptation to a parasitic plant

Host-parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR-Cas9-edited sorghum further indicate that the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

Coevolution Creates Complex Mosaics across Large Landscapes.

The spatial distribution of populations can influence the evolutionary outcome of species interactions. The variation in direction and strength of selection across local communities creates geographic selection mosaics that, when combined with gene flow and genomic processes such as genome duplication or hybridization, can fuel ongoing coevolution. A fundamental problem to solve is how coevolution proceeds when many populations that vary in their ecological outcomes are connected across large landscapes. Here we use a lattice model to explore this problem. Our results show that the complex interrelationships among the elements of the geographic mosaic of coevolution can lead to the formation of clusters of populations with similar phenotypes that are larger than expected by local selection. Our results indicate that neither the spatial distribution of phenotypes nor the spatial differences in magnitude and direction of selection alone dictate coevolutionary dynamics: the geographic mosaic of coevolution affects formation of phenotypic clusters, which in turn affect the spatial and temporal dynamics of coevolution. Because the formation of large phenotypic clusters depends on gene flow, we predict that current habitat fragmentation will change the outcomes of geographic mosaics, coupling spatial patterns in selection and phenotypes.

Geographical variation in cone traits of Pinus nigra as result of crossbill predation: implications for assisted migration

The interaction between Spanish Black pine (Pinus nigra subsp. salzmannii) and common crossbill (Loxia curvirostra) could have resulted in a geographic mosaic of coevolution in the Iberian Peninsula. In turn, this coevolutionary interaction might limit the future applicability of assisted migration as a tool to adapt forests of Spanish Black pine to ongoing climate change. Several cone and seed traits were measured in 740 cones collected at six stands distributed across the range of Spanish Black pine. Data were analysed by means of linear-mixed effects models, canonical analysis of principal coordinates and random-forest analysis. Results showed that cones from the northern pine populations exhibited more defensive traits against crossbill predation than cones from the central and southern populations, resulting in a geographic mosaic of selection. Assisted migration of P. nigra would involve moving southern populations toward the north of the species’ range and would result in introducing the genotypes of pines with poorly defended cones into areas where crossbills are comparatively more abundant. The resulting risks for the regeneration prospects of the translocated trees are discussed.

Geographic consistency and variation in conflicting selection generated by pollinators and seed predators.

Floral traits that attract pollinators may also attract seed predators, which, in turn, may generate conflicting natural selection on such traits. Although such selection trade-offs are expected to vary geographically, few studies have investigated selection mediated by pollinators and seed predators across a geographic mosaic of environments and floral variation. Floral traits were investigated in 14 populations of the bumble-bee-pollinated herb, Pedicularis rex, in which tubular flowers are subtended by cupular bracts holding rain water. To study potentially conflicting selection on floral traits generated by pollinators and florivores, stigmatic pollen loads, initial seed set, pre-dispersal seed predation and final viable seed production were measured in 12-14 populations in the field. Generalized Linear Model (GLM) analyses indicated that the pollen load on stigmas was positively related to the exsertion of the corolla beyond the cupular bracts and size of the lower corolla lip, but so too was the rate of seed predation, creating conflicting selection on both floral traits. A geographic mosaic of selection mediated by seed predators, but not pollinators, was indicated by significant variation in levels of seed predation and the inclusion of two-, three- and four-way interaction terms between population and seed predation in the best model [lowest corrected Akaike Information Criterion (AICc)] explaining final seed production. These results indicate opposing selection in operation: pollinators generated selection for greater floral exsertion beyond the bracts, but seed predators generated selection for reduced exsertion above the protective pools of water, although the strength of the latter varied across populations.

A geographic mosaic of trophic interactions and selection: trees, aphids and birds

Genetic variation in plants is known to influence arthropod assemblages and species interactions. However, these influences may be contingent upon local environmental conditions. Here, we examine how plant genotype-based trophic interactions and patterns of natural selection change across environments. Studying the cottonwood tree, Populus angustifolia, the galling aphid, Pemphigus betae and its avian predators, we used three common gardens across an environmental gradient to examine the effects of plant genotype on gall abundance, gall size, aphid fecundity and predation rate on galls. Three patterns emerged: (i) plant genotype explained variation in gall abundance and predation, (ii) G×E explained variation in aphid fecundity, and environment explained variation in gall abundance and gall size, (iii) natural selection on gall size changed from directional to stabilizing across environments.

Evolution of Complex Traits: The Case ofErysimumCorolla Shape

The evolution of flower shape has attracted the attention of biologists for at least two hundred years. Although much information is accumulating on the genetic architecture of flower shape, information on its adaptive significance is much scarcer. Using geometric morphometrics, we have explored the microevolution of corolla shape in Erysimum mediohispanicum during the past decade. We have found that, by contrast with conventional wisdom, corolla shape shows great variation even between co-occurring individuals. This variation can have strong fitness consequences, with reproductive success being associated with specific corolla shapes. Corolla shape seems to act in E. mediohispanicum as an honest signal, since it is associated with reward (nectar and pollen) and determines the preference pattern of important pollinators. Finally, since pollinator fauna varies geographically in this generalist plant species, we have detected a geographic mosaic of selection on E. mediohispanicum corolla shape in southeastern Spain that has resulted in a pattern of local adaptation. We hope that this review will encourage other evolutionary biologists to explore corolla shape microevolution, helping to unravel Darwin's “abominable mystery.”

Antagonistic Coevolution and Sex

One of the leading hypotheses for the maintenance of sexual reproduction is the Red Queen hypothesis. The underlying premise of the Red Queen hypothesis is that parasites rapidly evolve to infect common host genotypes. This response by parasites could result in the long-term maintenance of genetic variation and may favor sexual reproduction over asexual reproduction. The underlying ideas present a wonderful microcosm for teaching evolution. Here I present the reasons for why sex is anomalous for evolutionary theory, the rationale underlying the Red Queen hypothesis, and some empirical studies of the Red Queen hypothesis using a freshwater snail. The empirical results are consistent with the Red Queen hypothesis. In addition, the distribution of sexual and asexual reproduction in the snail leads naturally to thinking about coevolution in a geographic mosaic of parasite-mediated natural selection.

Fire Drives Transcontinental Variation in Tree Birch Defense against Browsing by Snowshoe Hares

Fire has been the dominant disturbance in boreal America since the Pleistocene, resulting in a spatial mosaic in which the most fire occurs in the continental northwest. Spatial variation in snowshoe hare (Lepus americanus) density reflects the fire mosaic. Because fire initiates secondary forest succession, a fire mosaic creates variation in the abundance of early successional plants that snowshoe hares eat in winter, leading to geographic variation in hare density. We hypothesize that fire is the template for a geographic mosaic of natural selection: where fire is greatest and hares are most abundant, hare browsing has most strongly selected juvenile-phase woody plants for defense. We tested the hypothesis at multiple spatial scales using Alaska birch (Betula neoalaskana) and white birch (Betula papyrifera). We also examined five alternative hypotheses for geographic variation in antibrowsing defense. The fire-hare-defense hypothesis was supported at transcontinental, regional, and local scales; alternative hypotheses were rejected. Our results link transcontinental variation in species interactions to an abiotic environmental driver, fire. Intakes of defense toxins by Alaskan hares exceed those by Wisconsin hares, suggesting that the proposed selection mosaic may coincide with a geographic mosaic of coevolution.

Interactions between Genetic Drift, Gene Flow, and Selection Mosaics Drive Parasite Local Adaptation

Interactions between gene flow, spatially variable selection, and genetic drift have long been a central focus of evolutionary research. In contrast, only recently has the potential importance of interactions between these factors for coevolutionary dynamics and the emergence of parasite local adaptation been realized. Here we study host-parasite coevolution in a metapopulation model when both the biotic and the abiotic components of the environment vary in space. We provide a general expression for parasite local adaptation that allows local adaptation to be partitioned into the contributions of spatial covariances between host and parasite genotype frequencies within and between habitats. This partitioning clarifies how relative rates of gene flow, spatially variable patterns of selection, and genetic drift interact to shape parasite local adaptation. Specifically, by using this expression in conjunction with coevolutionary models, we show that genetic drift can dramatically increase the level of parasite local adaptation under some models of specificity. We also show that the effect of migration on parasite local adaptation depends on the geographic mosaic of selection. We discuss how these predictions could be tested empirically or experimentally using microbial systems.

Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics.

BackgroundGeographic selection mosaics, in which species exert different evolutionary impacts on each other in different environments, may drive diversification in coevolving species. We studied the potential for geographic selection mosaics in plant-mycorrhizal interactions by testing whether the interaction between bishop pine (Pinus muricata D. Don) and one of its common ectomycorrhizal fungi (Rhizopogon occidentalis Zeller and Dodge) varies in outcome, when different combinations of plant and fungal genotypes are tested under a range of different abiotic and biotic conditions.ResultsWe used a 2 × 2 × 2 × 2 factorial experiment to test the main and interactive effects of plant lineage (two maternal seed families), fungal lineage (two spore collections), soil type (lab mix or field soil), and non-mycorrhizal microbes (with or without) on the performance of plants and fungi. Ecological outcomes, as assessed by plant and fungal performance, varied widely across experimental environments, including interactions between plant or fungal lineages and soil environmental factors.ConclusionThese results show the potential for selection mosaics in plant-mycorrhizal interactions, and indicate that these interactions are likely to coevolve in different ways in different environments, even when initially the genotypes of the interacting species are the same across all environments. Hence, selection mosaics may be equally as effective as genetic differences among populations in driving divergent coevolution among populations of interacting species.

Ecological and evolutionary consequences of spatial and temporal variation in pre-dispersal seed predation

Pre-dispersal seed predation may have important effects on population dynamics and trait evolution in plants. In this review, we first present a conceptual framework of the strength of pre-dispersal seed predation and its variation in space and time. We consider the interaction between plants and their seed predators to be “strong” when it affects plant population dynamics or causes changes in plant trait–fitness relationships, and “weak” when it has no such effects, and propose ways of how to adequately assess these effects. Second, we review the ecological literature between 1991 and 2005 to evaluate documented effects of pre-dispersal seed predation on plants and draw five major conclusions. (1) Pre-dispersal seed predation rates are usually low but sometimes high, and show a considerable variation in space and time. (2) Direct evidence suggests that pre-dispersal seed predation can have a significant effect on recruitment and plant population growth rate. Accumulating evidence of seed-limited recruitment suggests that such effects are common. (3) Pre-dispersal seed predation affects selection on several plant traits, such as flowering phenology and flower number, which are usually interpreted mainly in the context of plant–pollinator interactions. (4) The patterns of variation in the interactions between plants and pre-dispersal seed predators suggest that geographic selection mosaics may be common. (5) Although there are numerous studies estimating seed predation, there are still rather few studies that have aimed at examining the interaction explicitly in terms of effects on plant population dynamics and trait selection. From these we know that seed predators can have important, and often variable, effects on plant population dynamics and trait evolution. However, it still remains to assess how important they are across study systems and relative to other aspects of the plant's biotic and abiotic environment.

EVOLUTIONARY DIVERSIFICATION THROUGH HYBRIDIZATION IN A WILD HOST?PATHOGEN INTERACTION

Coevolutionary outcomes between interacting species are predicted to vary across landscapes, as environmental conditions, gene flow, and the strength of selection vary among populations. Using a combination of molecular, experimental, and field approaches, we describe how broad-scale patterns of environmental heterogeneity, genetic divergence, and regional adaptation have the potential to influence coevolutionary processes in the Linum marginale-Melampsora lini plant-pathogen interaction. We show that two genetically and geographically divergent pathogen lineages dominate interactions with the host across Australia, and demonstrate a hybrid origin for one of the lineages. We further demonstrate that the geographic divergence of the two lineages of M. lini in Australia is related to variation among lineages in virulence, life-history characteristics, and response to environmental conditions. When correlated with data describing regional patterns of variation in host resistance diversity and mating system these observations highlight the potential for gene flow and geographic selection mosaics to generate and maintain coevolutionary diversification in long-standing host-pathogen interactions.

The evolution of novel herbicide tolerance in a noxious weed: the geographic mosaic of selection

Understanding how genetic variation is organized over geography has long been of interest to evolutionary biologists given that traits can vary within and among populations, across regions, and at continental or global scales. The pattern of regional variation can have an important impact on trait evolution at the local or population level. Using a common garden, we asked whether a geographically variable mosaic of tolerance to the widely applied herbicide RoundUp® existed in two closely related co-occurring species of morning glory, Ipomoea purpurea and I. hederacea. We assayed RoundUp tolerance in over 1,700 plants representing 290 families from 29 populations in the southeastern United States. Our findings suggest that the two species of morning glory partition their respective levels of genetic variation for tolerance to glyphosate differently. Variation for tolerance in I. purpurea appears to exist among maternal lines and regions, whereas in I. hederacea, variation in tolerance existed only among populations. In addition, we find a significant hotspot of tolerance or positive spatial aggregation of this trait on a local scale in I. purpurea populations from the Coastal Plain. This suggests that either similar regimes of selection or gene flow between populations can produce a geographic mosaic of tolerance. These results highlight the fact that the genetic variation underlying an adaptive trait can exist at many different scales, whether it be within- or among-populations, among geographical ‘hotspots,’ or among distinct ecological regions. Given these results, the partitioning of genetic variation should be considered before making predictions about an adaptive trait’s evolutionary trajectory.

The geographic selection mosaic for squirrels, crossbills and Aleppo pine

The interactions between many species are structured in a geographic mosaic of populations among which selection is divergent. Here we tested the hypothesis that such a geographic selection mosaic arises for common crossbills (Loxia curvirostra) feeding on seeds in the cones of Aleppo pine (Pinus halepensis) because of geographic variation in the occurrence of European red squirrels (Sciurus vulgaris). On the Iberian Peninsula, Sciurus exerted directional selection favouring larger cones with larger scales, which has caused cones there to be larger than in the Balearic Islands where Sciurus are absent. Moreover, cones on the Iberian Peninsula are so large that they are apparently little used by the relatively small-billed crossbills on the Peninsula; selection by Sciurus seems to have made the cones so difficult to feed on that crossbills rely mostly on the seeds of other conifers. Where crossbills are present but Sciurus are absent (Mallorca Island), cones were smaller as a result of relaxation of selection by Sciurus. However, cones on Mallorca had proportionally thicker scales in comparison to where both Sciurus and crossbills are absent (Ibiza Island), presumably as an adaptation against crossbill predation. Here crossbills specialize on Aleppo pine, have relatively large bills and have apparently coevolved in an arms race with Aleppo pine. These results suggest that Sciurus has influenced both the geographic selection mosaics for crossbills and conifers and the adaptive radiation of crossbills in Eurasia much like Tamiasciurus has done in the North America.

The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine.

The geographic mosaic theory of coevolution posits that the form of selection between interacting species varies across a landscape with coevolution important and active in some locations (i.e., coevolutionary hotspots) but not in others (i.e., coevolutionary coldspots). We tested the hypothesis that the presence of red squirrels (Tamiasciurus hudsonicus) affects the occurrence of coevolution between red crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) and thereby provides a mechanism giving rise to a geographic mosaic of selection. Red squirrels are the predominant predispersal seed predator and selective agent on lodgepole pine cones. However, in four isolated mountain ranges east and west of the Rocky Mountains, red squirrels are absent and red crossbills are the main predispersal seed predator. These isolated populations of pine have apparently evolved without Tamiasciurus for about 10,000 to 12,000 years. Based on published morphological, genetic, and paleobotanical studies, we infer that cone traits in these isolated populations that show parallel differences from cones in the Rocky Mountains have changed in parallel. We used data on crossbill and conifer cone morphology and feeding preferences and efficiency to detect whether red crossbills and lodgepole pine exhibit reciprocal adaptations, which would imply coevolution. Cone traits that act to deter Tamiasciurus and result in high ratios of cone mass to seed mass were less developed in the isolated populations. Cone traits that act to deter crossbills include larger and thicker scales and perhaps increased overlap between successive scales and were enhanced in the isolated populations. In the larger, isolated mountain ranges crossbills have evolved deeper, shorter, and therefore more decurved bills to exploit these cones. This provides crossbills with higher feeding rates, and the change in bill shape has improved efficiency by reducing the concomitant increases in body mass and daily energy expenditures that would have resulted if only bill size had increased. These parallel adaptations and counter adaptations in red crossbills and lodgepole pine are interpreted as reciprocal adaptations and imply that these crossbills and pine are in coevolutionary arms races where red squirrels are absent (i.e., coevolutionary hotspots) but not where red squirrels are present (i.e., coevolutionary cold-spots).

THE INFLUENCE OF A COMPETITOR ON THE GEOGRAPHIC MOSAIC OF COEVOLUTION BETWEEN CROSSBILLS AND LODGEPOLE PINE

The geographic mosaic theory of coevolution posits that the form of selection between interacting species varies across a landscape with coevolution important and active in some locations (i.e., coevolutionary hotspots) but not in others (i.e., coevolutionary coldspots). We tested the hypothesis that the presence of red squirrels (Tamiasciurus hudsonicus) affects the occurrence of coevolution between red crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) and thereby provides a mechanism giving rise to a geographic mosaic of selection. Red squirrels are the predominant predispersal seed predator and selective agent on lodgepole pine cones. However, in four isolated mountain ranges east and west of the Rocky Mountains, red squirrels are absent and red crossbills are the main predispersal seed predator. These isolated populations of pine have apparently evolved without Tamiasciurus for about 10,000 to 12,000 years. Based on published morphological, genetic, and paleobotanical studies, we infer that cone traits in these isolated populations that show parallel differences from cones in the Rocky Mountains have changed in parallel. We used data on crossbill and conifer cone morphology and feeding preferences and efficiency to detect whether red crossbills and lodgepole pine exhibit reciprocal adaptations, which would imply coevolution. Cone traits that act to deter Tamiasciurus and result in high ratios of cone mass to seed mass were less developed in the isolated populations. Cone traits that act to deter crossbills include larger and thicker scales and perhaps increased overlap between successive scales and were enhanced in the isolated populations. In the larger, isolated mountain ranges crossbills have evolved deeper, shorter, and therefore more decurved bills to exploit these cones. This provides crossbills with higher feeding rates, and the change in bill shape has improved efficiency by reducing the concomitant increases in body mass and daily energy expenditures that would have resulted if only bill size had increased. These parallel adaptations and counter adaptations in red crossbills and lodgepole pine are interpreted as reciprocal adaptations and imply that these crossbills and pine are in coevolutionary arms races where red squirrels are absent (i.e., coevolutionary hotspots) but not where red squirrels are present (i.e., coevolutionary coldspots).