Chemical cues and genetic divergence in insects on plants: conceptual cross pollination between mutualistic and antagonistic systems

Segar, Simon T.; Volf, Martin; Sisol, Mentap; Pardikes, Nicholas A.; Souto‐Vilarós, Daniel

doi:10.1016/j.cois.2018.11.009

Cited by 8 publications

(10 citation statements)

References 67 publications

(72 reference statements)

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“…Reciprocal selection on signaling and defense traits has shaped the molecular constraints governing how antagonistic larvae develop into mutualistic adult pollinators 8,41 . In this study, our novel combination of classic electrophysiological experiments and multi-omics approaches has illuminated some key mechanisms forming the coadaptation in a pair of fig-pollinator mutualists.…”

Section: Discussionmentioning

confidence: 99%

Molecular mechanisms of mutualistic and antagonistic interactions in a plant–pollinator association

Wang

Yang

et al. 2021

Nat Ecol Evol

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Many insects metamorphose from antagonistic larvae into mutualistic adult pollinators, with reciprocal adaptation leading to specialized insect-plant associations.It remains unknown how such interactions are established at molecular level. Here we assembled high-quality genomes of a fig species, Ficus pumila var. pumila, and its specific pollinating wasp, Wiebesia pumilae. We combined multi-omics with validation experiments to reveal molecular mechanisms underlying this specialized interaction. In the plant, we identified the specific compound attracting pollinators and validated the function of several key genes regulating its biosynthesis. In the pollinator, we found a highly reduced number of odorant-binding protein (OBP) genes and an OBP mainly binding the attractant. During antagonistic interaction, we found similar chemical profiles and turnovers throughout the development of galled ovules and seeds, and a significant contraction of detoxification-related gene families in the pollinator. Our study detects some key genes bridging coevolved mutualists, establishing expectations for more diffuse insect-pollinator systems.

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Section: Discussionmentioning

confidence: 99%

Molecular mechanisms of mutualistic and antagonistic interactions in a plant–pollinator association

Wang

Yang

et al. 2021

Nat Ecol Evol

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“…While the genomic data for such analyses are becoming increasingly available (Mori et al, ; Xiao et al, ) they have yet to be compiled for our study system. Genomic matching of the corresponding genes in plants and pollinators stands out as the necessary next step toward the mechanistic understanding of cospeciation patterns (Segar et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Further research into the mechanisms, however, remains warranted. In particular, a definitive proof of cospeciation resulting from co‐evolution (e.g., rather than from similar responses to geographic isolation) would require demonstrating a match between the signal genes in figs (scent pathways) and receiver genes in wasps (olfactory receptors; Segar, Volf, Sisol, Pardikes, & Souto‐Vilarós, ). While the genomic data for such analyses are becoming increasingly available (Mori et al, ; Xiao et al, ) they have yet to be compiled for our study system.…”

Section: Discussionmentioning

confidence: 99%

Faster speciation of fig‐wasps than their host figs leads to decoupled speciation dynamics: Snapshots across the speciation continuum

et al. 2019

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Even though speciation involving multiple interacting partners, such as plants and their pollinators, has attracted much research, most studies focus on isolated phases of the process. This currently precludes an integrated understanding of the mechanisms leading to cospeciation. Here, we examine population genetic structure across six species‐pairs of figs and their pollinating wasps along an elevational gradient in New Guinea. Specifically, we test three hypotheses on the genetic structure within the examined species‐pairs and find that the hypothesized genetic structures represent different phases of a single continuum, from incipient cospeciation to the full formation of new species. Our results also illuminate the mechanisms governing cospeciation, namely that fig wasps tend to accumulate population genetic differences faster than their figs, which initially decouples the speciation dynamics between the two interacting partners and breaks down their one‐to‐one matching. This intermediate phase is followed by genetic divergence of both partners, which may eventually restore the one‐to‐one matching among the fully formed species. Together, these findings integrate current knowledge on the mechanisms operating during different phases of the cospeciation process. They also reveal that the increasingly reported breakdowns in one‐to‐one matching may be an inherent part of the cospeciation process. Mechanistic understanding of this process is needed to explain how the extraordinary diversity of species, especially in the tropics, has emerged. Knowing which breakdowns in species interactions are a natural phase of cospeciation and which may endanger further generation of diversity seems critical in a constantly changing world.

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“…Due to their relatively short generation times, some insects may rapidly develop HAD [23], with evidence suggesting that insects can evolve to exploit novel hosts within as little as 20 years (equivalent to 40 generations) [24]. Diverging host use across populations requires the evolution of differences in multiple traits related to detecting and responding to novel host-associated chemical cues [25]. In agroecosystems, HAD can influence populations of herbivorous insect pests and their associated natural enemies [23].…”

Section: Introductionmentioning

confidence: 99%

Improving Natural Enemy Selection in Biological Control through Greater Attention to Chemical Ecology and Host-Associated Differentiation of Target Arthropod Pests

Thompson

Medina

Helms

2022

Insects

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Host-associated differentiation (HAD) refers to cases in which genetically distinct populations of a species (e.g., herbivores or natural enemies) preferentially reproduce or feed on different host species. In agroecosystems, HAD often results in unique strains or biotypes of pest species, each attacking different species of crops. However, HAD is not restricted to pest populations, and may cascade to the third trophic level, affecting host selection by natural enemies, and ultimately leading to HAD within natural enemy species. Natural enemy HAD may affect the outcomes of biological control efforts, whether classical, conservation, or augmentative. Here, we explore the potential effects of pest and natural enemy HAD on biological control in agroecosystems, with emphases on current knowledge gaps and implications of HAD for selection of biological control agents. Additionally, given the importance of semiochemicals in mediating interactions between trophic levels, we emphasize the role of chemical ecology in interactions between pests and natural enemies, and suggest areas of consideration for biological control. Overall, we aim to jump-start a conversation concerning the relevance of HAD in biological control by reviewing currently available information on natural enemy HAD, identifying challenges to incorporating HAD considerations into biological control efforts, and proposing future research directions on natural enemy selection and HAD.

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Chemical cues and genetic divergence in insects on plants: conceptual cross pollination between mutualistic and antagonistic systems

Cited by 8 publications

References 67 publications

Molecular mechanisms of mutualistic and antagonistic interactions in a plant–pollinator association

Molecular mechanisms of mutualistic and antagonistic interactions in a plant–pollinator association

Faster speciation of fig‐wasps than their host figs leads to decoupled speciation dynamics: Snapshots across the speciation continuum

Improving Natural Enemy Selection in Biological Control through Greater Attention to Chemical Ecology and Host-Associated Differentiation of Target Arthropod Pests

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