Host-Associated Genetic Differentiation in Phytophagous Insects: General Phenomenon or Isolated Exceptions? Evidence From a Goldenrod-Insect Community

Stireman, John O.; Nason, John D.; Heard, Stephen B.

doi:10.1554/05-222.1

Cited by 171 publications

(174 citation statements)

References 65 publications

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“…However, this apparent rarity may reflect mostly a lack of data on levels of hybridization in a number of good candidate models (11). Additionally, genetic studies on species that are thought to be homogenous may reveal unsuspected genetic and ecological diversity in sympatry (42).…”

Section: Resultsmentioning

confidence: 99%

A continuum of genetic divergence from sympatric host races to species in the pea aphid complex

Peccoud¹,

Ollivier²,

Plantegenest

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

368

525

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Sympatric populations of insects adapted to different host plants, i.e., host races, are good models to investigate how natural selection can promote speciation in the face of ongoing gene flow. However, host races are documented in very few model systems and their gradual evolution into good species, as assumed under a Darwinian view of species formation, lacks strong empirical support. We aim at resolving this uncertainty by investigating host specialization and gene flow among populations of the pea aphid complex, Acyrthosiphon pisum. Genetic markers and tests of host plant specificity indicate the existence of at least 11 well-distinguished sympatric populations associated with different host plants in Western Europe. Population assignment tests show variable migration and hybridization rates among sympatric populations, delineating 8 host races and 3 possible species. Notably, hybridization correlates negatively with genetic differentiation, forming a continuum of population divergence toward virtually complete speciation. The pea aphid complex thus illustrates how ecological divergence can be sustained among many hybridizing populations and how insect host races blend into species by gradual reduction of gene flow. divergent selection ͉ ecological speciation ͉ hybridization ͉ sympatric speciation ͉ phytophagous insects T he beginning of this century has seen the reconciliation of Darwin's view that species gradually emerge by the primary action of natural selection, with the modern evolutionary synthesis defining speciation as the evolution of reproductive isolation (1-4). Adaptations to different habitats and resources may induce reproductive isolation (reviewed in refs. 1, 5, and 6) if morphology or niche selection determines mate choice and if hybrids between ecologically divergent taxa are unfit in the parental environments. Theoretical models and recent empirical studies (reviewed in refs. 7 and 8) have shown that these ecological reproductive barriers may evolve without the geographical separation of populations, an extrinsic barrier to hybridization (gene flow) that was long thought to be a requisite for speciation in animals (2). Divergence in sympatry (i.e., within the same region) implies a more gradual reduction of gene flow that should reflect increasing reproductive isolation and the continuum of speciation from polymorphic populations to good species. Such evolution is not observable in nature at reasonable timescales, but it could be inferred from the multiple stages of sympatric divergence observed within a variety of organisms (9). In phytophagous insects, ''host races'' constitute these intermediate stages of speciation. Host races refer to sympatric populations in partial reproductive isolation that are specialized to different host plants (10-12). Although host race formation can be rapid (12)(13)(14), their transition into full species and the reduction of gene flow during the final stages of speciation have remained difficult to trace. Host races are characterized in very few insect s...

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Section: Resultsmentioning

confidence: 99%

A continuum of genetic divergence from sympatric host races to species in the pea aphid complex

Peccoud¹,

Ollivier²,

Plantegenest

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

368

525

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show abstract

“…Although much of this argument has centered on the question of sympatric speciation (16), ''ecological speciation'' stemming from divergent ecological selection need not be sympatric (84,85). There is evidence for both allopatric and sympatric ecological speciation in phytophagous insects (17,86). Yet, among 145 pairs of presumptive sister species in 45 phylogenies, Winkler and Mitter (71) found divergence in host association in only 48%.…”

Section: Evolution Of Herbivoresmentioning

confidence: 99%

Macroevolution and the biological diversity of plants and herbivores

Futuyma

Agrawal

2009

Proc. Natl. Acad. Sci. U.S.A.

550

467

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Terrestrial biodiversity is dominated by plants and the herbivores that consume them, and they are one of the major conduits of energy flow up to higher trophic levels. Here, we address the processes that have generated the spectacular diversity of flowering plants (>300,000 species) and insect herbivores (likely >1 million species). Long-standing macroevolutionary hypotheses have postulated that reciprocal evolution of adaptations and subsequent bursts of speciation have given rise to much of this biodiversity. We critically evaluate various predictions based on this coevolutionary theory. Phylogenetic reconstruction of ancestral states has revealed evidence for escalation in the potency or variety of plant lineages' chemical defenses; however, escalation of defense has been moderated by tradeoffs and alternative strategies (e.g., tolerance or defense by biotic agents). There is still surprisingly scant evidence that novel defense traits reduce herbivory and that such evolutionary novelty spurs diversification. Consistent with the coevolutionary hypothesis, there is some evidence that diversification of herbivores has lagged behind, but has nevertheless been temporally correlated with that of their host-plant clades, indicating colonization and radiation of insects on diversifying plants. However, there is still limited support for the role of host-plant shifts in insect diversification. Finally, a frontier area of research, and a general conclusion of our review, is that community ecology and the long-term evolutionary history of plant and insect diversification are inexorably intertwined.coevolution ͉ herbivory ͉ insect host range ͉ phylogenetic analyses ͉ plant defense theory

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“…Failure to distinguish cryptic species underestimates species richness and distorts our perception of trends in diversity [4][5][6]. Additionally, pooling together cryptic species with distinct characteristics can obscure our understanding of each taxon's individual niche and function [1,[7][8][9][10][11][12]. These problems are further exacerbated by our incomplete understanding of the geographical distribution & 2016 The Author(s) Published by the Royal Society.…”

Section: Introductionmentioning

confidence: 99%

Cryptic species diversity reveals biogeographic support for the ‘mountain passes are higher in the tropics’ hypothesis

et al. 2016

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The 'mountain passes are higher in the tropics' (MPHT) hypothesis posits that reduced climate variability at low latitudes should select for narrower thermal tolerances, lower dispersal and smaller elevational ranges compared with higher latitudes. These latitudinal differences could increase species richness at low latitudes, but that increase may be largely cryptic, because physiological and dispersal traits isolating populations might not correspond to morphological differences. Yet previous tests of the MPHT hypothesis have not addressed cryptic diversity. We use integrative taxonomy, combining morphology (6136 specimens) and DNA barcoding (1832 specimens) to compare the species richness, cryptic diversity and elevational ranges of mayflies (Ephemeroptera) in the Rocky Mountains (Colorado; approx. 408N) and the Andes (Ecuador; approx. 08). We find higher species richness and smaller elevational ranges in Ecuador than Colorado, but only after quantifying and accounting for cryptic diversity. The opposite pattern is found when comparing diversity based on morphology alone, underscoring the importance of uncovering cryptic species to understand global biodiversity patterns.

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Host-Associated Genetic Differentiation in Phytophagous Insects: General Phenomenon or Isolated Exceptions? Evidence From a Goldenrod-Insect Community

Cited by 171 publications

References 65 publications

A continuum of genetic divergence from sympatric host races to species in the pea aphid complex

A continuum of genetic divergence from sympatric host races to species in the pea aphid complex

Macroevolution and the biological diversity of plants and herbivores

Cryptic species diversity reveals biogeographic support for the ‘mountain passes are higher in the tropics’ hypothesis

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