Wing plasticity and associated gene expression varies across the pea aphid biotype complex

Parker, Benjamin J.; Driscoll, Rose M.H.; Grantham, Mary E.; Hrček, Jan; Brisson, Jennifer A.

doi:10.1111/evo.14174

Cited by 10 publications

(11 citation statements)

References 48 publications

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“…Most challenges to Dollo's law come from macroevolutionary approaches and include a large number of examples, such as shell coiling in limpets (Collin and Cipriani 2003), compound eyes in ostracods (Syme and Oakley 2012), sex and parasitism in mites (Klimov and O'Connor 2013;Domes et al 2007), mandibular teeth in frogs (Wiens 2011), limb evolution (Kohlsdorf and Wagner 2006), eggshells and oviparity (Lynch and Wagner 2010;Recknagel et al 2018;Esquerré et al 2020) in Squamata. At the same time, several possible mechansisms underlying the reversible evolution of complex traits, have been proposed, including phenotypic plasticity (Visser et al 2021;Parker et al 2021) and reticulate evolution (Horreo et al 2020). Examples of compensatory mutations which have been able to rescue the once-lost functionality of genes have also been found (Esfeld et al 2018) and it has been observed that a reversal to a lost ancestral state could happen through changes in relatively few genes (Seher et al 2012).…”

Section: Introductionmentioning

confidence: 99%

Macroevolutionary Analyses Provide New Evidences of Phasmid Wings Evolution as a Reversible Process

Forni

Martelossi

Valero³

et al. 2020

Preprint

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The concept that complex ancestral traits can never be re-acquired after their loss has grown popular since its initial formulation and is often referred to as Dollo's law. Nonetheless, several macroevolutionary evidences - along with molecular ones - suggest instances where complex phenotypes could have been lost throughout a clade evolutionary history and subsequently reverted to their former state in derived lineages. One of the first and most notable rejection of Dollo's law is represented by wing evolution in phasmids: this polyneopteran order of insects - which comprises stick and leaf insects - has played a central role in initiating a long-standing debate on the topic. In this study, a new and comprehensive molecular phylogeny of over 300 Phasmatodea species is used as a framework for investigating wing's evolutionary patterns in the clade, taking into consideration several sources of uncertainty and all the methodological recommendations which have been proposed to test Dollo's law rejection. Macroevolutionary analyses support a dynamic and reversible evolution of wings, with multiple transitions to ancestral states taking place after their loss. Our findings suggest that neither wings or flight have acted as drivers of Phasmatodea species diversification and that brachyptery is an unstable state, when not co-opted for non-aerodynamic adaptations. We also explored the impact on our results of different assumptions relative to the probability of reversals and losses: we found that until reversals are assumed over 30 times more unlikely than losses, they are consistently inferred despite uncertainty in tree and model parameters. Our findings demonstrate that wings evolution can be a reversible and dynamic process in phasmids and contribute to shape our understanding of complex phenotypes evolution.

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Section: Introductionmentioning

confidence: 99%

Macroevolutionary Analyses Provide New Evidences of Phasmid Wings Evolution as a Reversible Process

Forni

Martelossi

Valero³

et al. 2020

Preprint

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“…For instance, activation of TOR activity in honeybees is responsible for the developmental transition from facultatively sterile workers to reproductive queens, while repressing TOR activity could induce worker characters in queen-destined individuals ( Michalak et al, 2007 ). Transcriptomic analysis in maternal crowding of pea aphids suggested that genes functionally related to TOR signaling pathway were differentially expressed in mother aphids ( Parker et al, 2021 ). We therefore hypothesized that the canonical pathway of TOR-REPTOR-autophagy may be responsible for developmental plasticity of the wing disc in aphids, in accordance with lower TOR abundance in wingless-destined morph.…”

Section: Discussionmentioning

confidence: 99%

A novel gene REPTOR2 activates the autophagic degradation of wing disc in pea aphid

Yuan

Guo

Chen

et al. 2023

eLife

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Wing dimorphism in insects is an evolutionarily adaptive trait to maximize insect fitness under various environments, by which the population could be balanced between dispersing and reproduction. Most studies concern the regulatory mechanisms underlying the stimulation of wing morph in aphids, but relatively little research addresses the molecular basis of wing loss. Here, we found that, while developing normally in winged-destined pea aphids, the wing disc in wingless-destined aphids degenerated 30-hr postbirth and that this degeneration was due to autophagy rather than apoptosis. Activation of autophagy in first instar nymphs reduced the proportion of winged aphids, and suppression of autophagy increased the proportion. REPTOR2, associated with TOR signaling pathway, was identified by RNA-seq as a differentially expressed gene between the two morphs with higher expression in the thorax of wingless-destined aphids. Further genetic analysis indicated that REPTOR2 could be a novel gene derived from a gene duplication event that occurred exclusively in pea aphids on autosome A1 but translocated to the sex chromosome. Knockdown of REPTOR2 reduced autophagy in the wing disc and increased the proportion of winged aphids. In agreement with REPTOR’s canonical negative regulatory role of TOR on autophagy, winged-destined aphids had higher TOR expression in the wing disc. Suppression of TOR activated autophagy of the wing disc and decreased the proportion of winged aphids, and vice versa. Co-suppression of TOR and REPTOR2 showed that dsREPTOR2 could mask the positive effect of dsTOR on autophagy, suggesting that REPTOR2 acted as a key regulator downstream of TOR in the signaling pathway. These results revealed that the TOR signaling pathway suppressed autophagic degradation of the wing disc in pea aphids by negatively regulating the expression of REPTOR2.

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Section: Discussionmentioning

confidence: 99%

A Novel Gene REPTOR2 Activates the Autophagic Degradation of Wing Disc in Pea Aphid

Yuan

Guo²,

Chen

et al. 2022

Preprint

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Wing dimorphism is an evolutionarily adaptive trait to maximize insect fitness under various environments, by which the population could be balanced between migration and reproduction. Most studies concern the regulatory mechanisms underlying the stimulation of wing morph in aphids, but relatively little research addresses the molecular basis of wing loss. Here, we found that the wing disc of wingless-destined pea aphids degenerated 30 h post birth by autophagic rather than apoptotic degeneration, whereas winged-destined aphids developed normally. Activation of autophagy in 1st instar nymphs reduced the proportion of winged aphids, and suppression of autophagy increased the proportion. The REPTOR2 gene associated with TOR signaling pathway was identified by RNA-seq as a differentially expressed gene between the two morphs, with higher expression in the thorax of wingless-destined aphids. Further genetic analysis indicated that REPTOR2 could be a novel gene derived from a gene duplication event exclusively in pea aphid on autosome A1 but translocated to the sex chromosome. Knockdown of REPTOR2 reduced autophagy in the wing disc and increased the proportion of winged aphids. In agreement with REPTOR's canonical negative regulatory role of TOR on autophagy, winged-destined aphids had higher TOR expression in the wing disc. Suppression of TOR activated autophagy of the wing disc and decreased the proportion of winged aphids, and vice versa. These results revealed that the TOR signaling pathway controlled degradation of the wing disc in pea aphids, and that REPTOR2 could modulate this autophagic degradation.

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Wing plasticity and associated gene expression varies across the pea aphid biotype complex

Cited by 10 publications

References 48 publications

Macroevolutionary Analyses Provide New Evidences of Phasmid Wings Evolution as a Reversible Process

Macroevolutionary Analyses Provide New Evidences of Phasmid Wings Evolution as a Reversible Process

A novel gene REPTOR2 activates the autophagic degradation of wing disc in pea aphid

A Novel Gene REPTOR2 Activates the Autophagic Degradation of Wing Disc in Pea Aphid

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