Insights into the Interaction between the Monophagous Tephritid Fly Anastrepha acris and its Highly Toxic Host Hippomane mancinella (Euphorbiaceae)

Aluja, Martı́n; Pascacio-Villafán, Carlos; Altúzar-Molina, Alma; Monribot‐Villanueva, Juan L.; Guerrero‐Analco, José A.; Enciso, E. Grana; Ortega, Rafael; Acosta, Emilio; Guillén, Larissa

doi:10.1007/s10886-020-01164-8

Cited by 5 publications

(13 citation statements)

References 63 publications

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“…Larvae live confined within their host fruit until they complete their development, at which moment they normally exit the fruit to bury into the ground to metamorphose into pupae (Aluja et al., 2005). Larval development largely depends on the biochemical and nutritional characteristics of the host (Aluja & Mangan, 2008; Aluja et al., 2020; Balagawi et al., 2005; Oroño et al., 2019; Wu et al., 2011), which vary substantially among plant species and across different parts and different maturing and ripening stages of a single fruit (Birke et al., 2015; Fernandes‐da‐Silva & Zucoloto, 1993; Hafsi et al., 2016; Oroño et al., 2019). When hosts are scarce, females become habituated to host marking pheromones deposited on the fruit surface by previous ovipositing females, and a single fruit can be oviposited several times by the same or different females (Burrack et al., 2009; Lalonde & Mangel, 1994; Papaj & Aluja, 1993; Papaj et al., 1992).…”

Section: Introductionmentioning

confidence: 99%

“…The relationships of tephritid fruit fly larvae with their host and with other larvae are of utmost importance in the dynamics of competitive interactions and influence the organization and function of their communities (Aluja & Mangan, 2008; Aluja et al., 2020; Hafsi et al., 2016). To improve our understanding of the mechanisms behind changes in population dynamics and community composition in insect species whose larvae live confined and feed in isolated and ephemeral resources (such as tephritid flies), an integrative approach is needed leading to an examination of how insects respond when they consume diets with a wide range of macronutrient contents at varying conspecific densities and the identification of the sorts of environments that select for optimal functional traits and performance (Brousseau et al., 2018).…”

Section: Introductionmentioning

confidence: 99%

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Diet quality and conspecific larval density predict functional trait variation and performance in a polyphagous frugivorous fly

et al. 2022

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Diet quality and the presence and abundance of conspecifics feeding on the same food resource are critical factors that affect functional traits of many animal species and influence ecological processes. We hypothesized that in insects whose larvae live in groups of varying sizes in ephemeral and nutritionally variable environments, extreme macronutrient content in the feeding substrate is a barrier for optimal performance that can be overcome by the collective feeding behaviour of large numbers of larvae. We experimentally examined how multiple immature and adult traits of the polyphagous tephritid fruit fly, Anastrepha ludens, vary as a function of the quality of its larval diet (protein + carbohydrate [P + C] content of 8.0%–12.6% w/w, and protein‐to‐carbohydrate [P/C] ratio of 1.8–0.11) across extreme levels of conspecific larval densities (60–600 larvae/60 g of diet). Overall, we found positive effects on survival of immature and adult stages, the duration of the larval stage, pupal weight and adult emergence of flies, as dietary P + C content increased, followed by negative effects when the diet had extremely high carbohydrate‐biased macronutrient content. Larval density had positive, negative and curvilinear effects depending on the macronutrient composition of the food, resulting in a range of fly responses through a continuous scale of macronutrient content and larval density combinations. Optimal performance of A. ludens, in terms of larval development time, body weight and survival to adulthood, was found when the diet consisted of low P + C content and high P/C ratios, and low larval densities. Our findings point to a diet‐mediated relationship between density and survival to the adult stage, suggesting that large numbers (up to a point) of larvae can balance negative effects of conspecific competition when food is characterised by high macronutrient content and low P/C ratios. We conclude that diet quality and conspecific density interact in complex ways to shape trait expression and performance in a frugivorous fly. Addressing this interaction is key to advance the understanding of the mechanisms behind changes in population dynamics in insect species living in groups confined in isolated and ephemeral resources. Read the free Plain Language Summary for this article on the Journal blog.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Diet quality and conspecific larval density predict functional trait variation and performance in a polyphagous frugivorous fly

et al. 2022

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“…Our results implied that these plant secondary metabolites were vitally important for unripe citrus fruit defence against B. minax larvae. Similarly, research on the interactions among Anastrepha acris and its highly toxic host plant Hippomane mancinella indicated that phenylpropanoids, avonoids, chalcones and coumarins induced defence responses (Aluja et al, 2020). Taken together, these ndings open a window for further study on the induced defence mechanisms of unripe citrus fruits.…”

Section: Discussionmentioning

confidence: 87%

New Insights Into the Biological Interaction Between Unripe Citrus Fruits and the Tephritid Fly Bactrocera Minax Based on Omics

Zhang¹,

Xu²,

Wang³

et al. 2021

Preprint

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The adaptation of phytophagous insects to host defence is an important aspect of plant-insect interactions. The reciprocal adaptability between specialist insects and their hosts have been adequately explored; however, the mechanisms underlying the adaptation of tephritid fruit fly specialists, a group of notorious pests worldwide, to unripen host fruits remain elusive. Here, plant metabolomes and insect transcriptomes were analysed for the first time to explore the interaction between unripe citrus fruits and the Chinese citrus fly Bactrocera minax. Seventeen citrus secondary metabolites, mainly flavones, alkaloids and phenylpropanoids, were identified in the unripe citrus fruit metabolome and they accumulated during larval feeding. Three detoxification genes (1 P450 gene, 2 ABCs genes) were highly expressed in B. minax larvae collected from unripe citrus fruits compared with the ones fed on artificial diets and ripe citrus fruits. Based on omics data, a novel ABC gene was screened through plant allelopathy tests and the gene was significantly upregulated in B. minax larvae treated with defensive secondary metabolites; additionally, the mortality rate of the larvae reached 51% after silencing the ABC gene by RNAi technique. Overall, these results shed light on the mechanisms underlying the biological interactions between tephritid fruit fly specialists and host fruits.

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“…striata ) was recently reported ( Ochoa-Sánchez et al, 2022 ). Here we chose as study model another fruit fly species adapted to monophagy: Anastrepha acris Stone (Diptera: Tephritidae), which is phylogenetically very close to A. ludens ( Mengual et al, 2017 ), but exclusively infests fruits of Hippomane mancinella L (Malpighiales: Euphorbiaceae) ( Aluja and Norrbom, 2000 ; Aluja et al, 2020 ). Hippomane mancinella is a tree that produces a fruit commonly known as “Apple of Death", which is highly toxic to many animals, including humans and insects ( Rao, 1974 ; Adolf and Hecker, 1984 ).…”

Section: Introductionmentioning

confidence: 99%

“…Recently, Aluja et al (2020) analyzed the interaction between H. mancinella, A. acris, and A. ludens , and found that diets enriched with different concentrations of dried fruit pulp of H. mancinella have a differential effect on the development of the larvae of both species. Not surprisingly, in A. ludens they found that H. mancinella produces a more pronounced, negative impact on larvae development as there is no natural association between the fly and this toxic fruit in nature.…”

Section: Introductionmentioning

confidence: 99%

Insights into the differences related to the resistance mechanisms to the highly toxic fruit Hippomane mancinella (Malpighiales: Euphorbiaceae) between the larvae of the sister species Anastrepha acris and Anastrepha ludens (Diptera: Tephritidae) through comparative transcriptomics

García-Saldaña,

Cerqueda-García,

Ibarra-Laclette

et al. 2024

Front. Physiol.

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The Manchineel, Hippomane mancinella (“Death Apple Tree”) is one of the most toxic fruits worldwide and nevertheless is the host plant of the monophagous fruit fly species Anastrepha acris (Diptera: Tephritidae). Here we aimed at elucidating the detoxification mechanisms in larvae of A. acris reared on a diet enriched with the toxic fruit (6% lyophilizate) through comparative transcriptomics. We compared the performance of A. acris larvae with that of the sister species A. ludens, a highly polyphagous pest species that is unable to infest H. mancinella in nature. The transcriptional alterations in A. ludens were significantly greater than in A. acris. We mainly found two resistance mechanisms in both species: structural, activating cuticle protein biosynthesis (chitin-binding proteins likely reducing permeability to toxic compounds in the intestine), and metabolic, triggering biosynthesis of serine proteases and xenobiotic metabolism activation by glutathione-S-transferases and cytochrome P450 oxidoreductase. Some cuticle proteins and serine proteases were not orthologous between both species, suggesting that in A. acris, a structural resistance mechanism has been selected allowing specialization to the highly toxic host plant. Our results represent a nice example of how two phylogenetically close species diverged over recent evolutionary time related to resistance mechanisms to plant secondary metabolites.

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Insights into the Interaction between the Monophagous Tephritid Fly Anastrepha acris and its Highly Toxic Host Hippomane mancinella (Euphorbiaceae)

Cited by 5 publications

References 63 publications

Diet quality and conspecific larval density predict functional trait variation and performance in a polyphagous frugivorous fly

Diet quality and conspecific larval density predict functional trait variation and performance in a polyphagous frugivorous fly

New Insights Into the Biological Interaction Between Unripe Citrus Fruits and the Tephritid Fly Bactrocera Minax Based on Omics

Insights into the differences related to the resistance mechanisms to the highly toxic fruit Hippomane mancinella (Malpighiales: Euphorbiaceae) between the larvae of the sister species Anastrepha acris and Anastrepha ludens (Diptera: Tephritidae) through comparative transcriptomics

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