skip to main content

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

We identified a geographic mosaic ofEurosta solidaginisfly 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‐plantSolidago altissimaproduced 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 ofE. solidaginishave 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 ofE. solidaginisform a mosaic hybrid zone in this region.

more » « less
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Reciprocal adaptation is the hallmark of arms race coevolution. Local coadaptation between natural enemies should generate a geographic mosaic pattern where both species have roughly matched abilities across their shared range. However, mosaic variation in ecologically relevant traits can also arise from processes unrelated to reciprocal selection, such as population structure or local environmental conditions. We tested whether these alternative processes can account for trait variation in the geographic mosaic of arms race coevolution between resistant garter snakes (Thamnophis sirtalis) and toxic newts (Taricha granulosa). We found that predator resistance and prey toxin levels are functionally matched in co-occurring populations, suggesting that mosaic variation in the armaments of both species results from the local pressures of reciprocal selection. By the same token, phenotypic and genetic variation in snake resistance deviates from neutral expectations of population genetic differentiation, showing a clear signature of adaptation to local toxin levels in newts. Contrastingly, newt toxin levels are best predicted by genetic differentiation among newt populations, and to a lesser extent, by the local environment and snake resistance. Exaggerated armaments suggest that coevolution occurs in certain hotspots, but prey population structure seems to be of particular influence on local phenotypic variation in both species throughout the geographic mosaic. Our results imply that processes other than reciprocal selection, like historical biogeography and environmental pressures, represent an important source of variation in the geographic mosaic of coevolution. Such a pattern supports the role of “trait remixing” in the geographic mosaic theory, the process by which non-adaptive forces dictate spatial variation in the interactions among species.

    more » « less
  2. Abstract

    Hybrid zones are geographic regions where isolating barriers between divergent populations are challenged by admixture. Identifying factors that facilitate or inhibit hybridization in sympatry can illuminate the processes that maintain those reproductive barriers. We analysed patterns of hybridization and phenotypic variation across two newly discovered hybrid zones between three subspecies of barn swallow (Hirundo rustica). These subspecies differ in ventral coloration and wing length, traits that are targets of sexual and natural selection, respectively, and are associated with genome‐wide differentiation in allopatry. We tested the hypothesis that the degree of divergence in these traits is associated with the extent of hybridization in secondary contact. We applied measures of population structure based on >23,000SNPs to confirm that named subspecies correspond to distinct genomic clusters, and assessed coincidence between geographic clines for ancestry and phenotype. Although gene flow was ongoing across both hybrid zones and pairwiseFSTbetween subspecies was extremely low, we found striking differences in the extent of hybridization. In the more phenotypically differentiated subspecies pair, clines for ancestry, wing length and ventral coloration were steep and coincident, suggestive of strong isolation and, potentially, selection associated with phenotype. In the less phenotypically differentiated pair, gene flow and phenotypic variation occurred over a wide geographic span, indicative of weaker isolation. Traits associated with genome‐wide differentiation in allopatry may thus also contribute to isolation in sympatry. We discuss potentially important additional roles for evolutionary history and ecology in shaping variation in the extent hybridization between closely related pairs of subspecies.

    more » « less
  3. Abstract

    Antagonistic coevolution between natural enemies can produce highly exaggerated traits, such as prey toxins and predator resistance. This reciprocal process of adaptation and counter‐adaptation may also open doors to other evolutionary novelties not directly involved in the phenotypic interface of coevolution. We tested the hypothesis that predator–prey coevolution coincided with the evolution of conspicuous coloration on resistant predators that retain prey toxins. In western North America, common garter snakes (Thamnophis sirtalis) have evolved extreme resistance to tetrodotoxin (TTX) in the coevolutionary arms race with their deadly prey, Pacific newts (Tarichaspp.). TTX‐resistant snakes can retain large amounts of ingested TTX, which could serve as a deterrent against the snakes' own predators if TTX toxicity and resistance are coupled with a conspicuous warning signal. We evaluated whether arms race escalation covaries with bright red coloration in snake populations across the geographic mosaic of coevolution. Snake colour variation departs from the neutral expectations of population genetic structure and covaries with escalating clines of newt TTX and snake resistance at two coevolutionary hotspots. In the Pacific Northwest, bright red coloration fits an expected pattern of an aposematic warning to avian predators: TTX‐resistant snakes that consume highly toxic newts also have relatively large, reddish‐orange dorsal blotches. Snake coloration also seems to have evolved with the arms race in California, but overall patterns are less intuitively consistent with aposematism. These results suggest that interactions with additional trophic levels can generate novel traits as a cascading consequence of arms race coevolution across the geographic mosaic.

    more » « less
  4. Introduction Plants and their insect herbivores represent a large fraction of the species in Amazonian forests and are often directly implicated in the origin and maintenance of biodiversity at local and regional scales. How these interactions may change over geographic distance is unknown because very few studies have investigated the herbivore fauna and defense chemicals of any host plant species at multiple sites in tropical forests. One hypothesis, the Geographic Mosaic Theory of Coevolution, predicts that if herbivore assemblages turn over in different parts of a plant’s range, then plant defense chemicals should also change, reflecting local selection pressures. Methods We tested this theory by studying 12 species of Protium (Burseraceae) trees that occur in both Iquitos, Peru, and Manaus, Brazil, in rainforests separated by 1500 km. We surveyed all insects observed directly feeding on the plants in both locations for 48 weeks in Manaus and 64 weeks in Iquitos. We analyzed the secondary metabolites in the leaves of all species in both locations using GC/MS and HPLC. Results and Discussion Although in both locations we found that Protium herbivores were dominated by insects from the orders Hemiptera, Coleoptera and Lepidoptera, we found almost complete turnover in the herbivore species composition in the two sites, and each host plant species had a different assemblage of herbivores in each location. Comparing the phylogenetic beta-diversity, we found low similarity in herbivore phylogenetic relatedness between host plant species in the two locations. However, the secondary metabolites found within a Protium species were similar across the two locations. We found no strong evidence that individuals from a host plant species in Iquitos or Manaus expressed locally-adapted defense chemicals, as individuals from geographic locations did not form clusters when looking at patterns of chemical similarity. These results are not consistent with the Geographic Mosaic Theory of Coevolution. The most intriguing pattern we found was a strong correlation between the diversity of herbivores per host plant species in both locations. We also found that plants with high chemical richness had lower numbers of herbivore species and numbers of total herbivores in both locations. We conclude that high chemical diversity is the most effective strategy for Protium trees to reduce insect herbivore attacks. We speculate that each secondary metabolite is effective at repelling only a few insect herbivores, and that different chemicals are likely effective in different parts of a plants’ geographic range. Future studies should investigate additional locations and additional natural enemies (i.e., fungal pathogens) to test the hypothesis that chemical diversity reduces attack from natural enemies and may explain the ecological and evolutionary success of rainforest trees over time and space. 
    more » « less
  5. 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 cropSorghum bicolor(L.) Moench and its association with the parasitic weedStriga 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 sorghumLOW GERMINATION STIMULANT 1 (LGS1)are broadly distributed among African landraces and geographically associated withS. hermonthicaoccurrence. However, low frequency of these alleles withinS. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation.LGS1is 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 surroundingLGS1and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit ofLGS1-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.

    more » « less