Flight ability is a great evolutionary success for animals that favors seeking new habitats, mates, and food resources (Roff, 1990). The loss of such ability has occurred in numerous insects (Roff, 1990; Harrison, 1980; Roff and Fairbairn, 1991). The wingless morph has evolved to optimize resource allocation from dispersal to reproduction, which facilitates population expansion under suitable conditions (Zera and Denno, 1997; Mole and Zera, 1993). Alternation between the wing morphs in aphid offspring is strongly influenced by maternal experience (Braendle et al., 2006). Pea aphids are recognized as a compelling laboratory model to study regulatory mechanisms underlying wing dimorphism, most notably through maternal population density (herein refers to as maternal density). It has been shown that ecdysteroids, miR-9b-ABCG4-insulin signaling, and two laterally transferred viral genes (Apns-1 and Apns-2) are responsible for producing winged offspring in parthenogenetic females (Vellichirammal et al., 2017; Shang et al., 2020; Parker and Brisson, 2019). Nevertheless, the phylogenetic evidence suggests that winged morph in aphids is a default developmental pattern, while the wingless morph is secondarily derived, from their winged ancestor (Braendle et al., 2006; Miyazaki, 1987). Thus, how wingless morph is controlled under favorable conditions needs to be studied, as such information will help to elucidate the differentiation of wing dimorphism in aphids.

Tissue degradation is a common developmental process in insects executed by programmed cell death (PCD), such as autophagy and apoptosis (Xu et al., 2019). During metamorphosis, Drosophila salivary glands, midgut and other larval tissues are removed by PCD (Xu et al., 2019). For example, suppression of apoptosis or autophagy or both could delay the degeneration of salivary glands (Berry and Baehrecke, 2007). Suppressing autophagy, but not apoptosis, severely interferes with the removal of the midgut during metamorphosis (Denton et al., 2012). These findings suggest that tissue-specific degeneration required different types of PCD. Furthermore, histological examinations in pea aphids show that the second instar nymphs of the winged-destined morph obviously possess a pair of wing discs, whereas wingless-destined morph does not (Ishikawa et al., 2008; Ogawa and Miura, 2013). Since the wing bud and the full wing are developed from the wing disc, it would be interesting to know whether and how PCD controls the fate of the wing disc cells, ultimately resulting in the wingless morph.

The evolutionarily conserved nutrient-sensing TOR (the target of rapamycin) pathway has been implicated in regulation of fecundity, life span as well as tissues degradation of insects under different nutritional conditions (Xu et al., 2019; Katewa and Kapahi, 2011). TOR coordinately regulates the balance between growth and autophagy in response to cellular and physiological conditions as well as environmental stresses such as intracellular amino acid availability and accessible energy levels (Saxton and Sabatini, 2017). Shortage of dietary amino acid depletion or starvation, inhibits TOR activity, which is known as a crucial step for autophagy induction in eukaryotes (Shimobayashi and Hall, 2016). Downregulation of TOR signaling pathway seems to be necessary for autophagic degradation to occur in different insect tissues such as the salivary gland and midgut (Berry and Baehrecke, 2007; Denton et al., 2012). TOR suppresses autophagy by directly phosphorylating multiple residues of autophagy-related proteins or repressing the transcription of autophagy-related genes. TOR phosphorylates Atg13, causing reduced affinity between Atg1 and its binding proteins and subsequently repressed autophagy (Puente et al., 2016). Alternatively, TOR also phosphorylates Ser527 and Ser530 of REPTOR (repressed by TOR) to prevent its entry into nucleus where REPTOR targets autophagy-related genes and suppresses their expression (Tiebe et al., 2015). In this study, we identify a novel gene REPTOR2 in pea aphids by comparing the transcriptome of wingless-destined versus winged-destined aphids at 24-hr postbirth. Since REPTOR2 has a higher expression in thorax of wingless-destined aphids, we hypothesized that REPTOR2 activates autophagic degradation in the wing disc to produce the wingless morph. Likewise, winged-destined aphids have a stronger TOR activity to suppress autophagy in the wing disc to develop into full wings. Experimentally, we specifically determined: (i) the time point to initiate PCD in the wing disc, (ii) the PCD type that was responsible for wing disc degeneration, and (iii) the role of REPTOR2 and TOR signaling cascade in determination wing dimorphism.

The wing disc consists of undifferentiated and proliferating cells designated to develop into a full insect wing during the nymphal stage (Neto-Silva et al., 2009). Fate of the wing disc is presumably determined by maternal signals triggered by environmental signals such as population density, physical contact, and the presence of natural enemies, as wing dimorphism in aphids is transgenerational (Braendle et al., 2006). It has been reported that ecdysteroids and miR-9b are the molecules that transduce maternal crowding signals to embryos, leading to a high proportion of winged offspring (Vellichirammal et al., 2017; Shang et al., 2020). However, few studies have focused on the role of the wing disc degradation at the onset of the nymphal stage in forming wing dimorphism. In this study, we demonstrated that a novel gene REPTOR2, highly expressed in the first instar nymphs of wingless-destined pea aphid morph 12-h postbirth, activated autophagy in the wing disc and resulted in its degeneration as early as 30-h postbirth. Different types of PCD have been reported to activate in tissue degeneration in many insect orders (Xu et al., 2019). Wing discs of soldier ant and some sex-dependent wingless morphs of lepidopterans are degenerated by apoptotic cell death (Fujiwara and Ogai, 2001; Niitsu, 2001; Sameshima et al., 2004; Rajakumar et al., 2012; Rajakumar et al., 2018). On the other hand, apoptosis did not seem to be necessary in wing disc degradation in aphids. Instead, typical features of autophagic cell death occurred at 30-h postbirth in wingless-destined morphs. Our results supported a model concerning aphid wing disc degeneration and development: Once experienced crowding, maternal aphids increased TOR expression in first instar nymphs. This was followed by the repression of REPTOR2 and autophagic degradation in the wing disc, thereby causing a high proportion of winged offspring. For the solitary maternal group on the other hand, TOR activity was arrested in the first instar offspring, and REPTOR2 and autophagy were subsequently activated in wing disc, leading to a high proportion of wingless offspring (Figure 5). Given the high expression in thorax of wingless-destined morph at early first instar nymphal stage, it was likely that REPTOR2 transduced the TOR signaling to activate autophagic degeneration of the wing disc in a tissue-specific manner.

Figure 5

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The TOR signaling pathway has been reported to modulate developmental plasticity in some insects (Koyama et al., 2013). 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. Suppression of TOR in Drosophila upregulates the expression of autophagy-related genes via phosphorylation of Ser527 and Ser530 in REPTOR (Tiebe et al., 2015). Similarly, pea aphid REPTOR2 is predicted to contain a conserved BRLZ domain that is capable of binding to GTAAACAA, the binding motif of FOXO as well (Tiebe et al., 2015). FOXO is a transcription factor that relays the insulin signaling to insect wing dimorphism. In the planthopper, activating insulin signaling transforms short-winged to long-winged morph via repressing the FOXO activity (Xu et al., 2015). Activation of FOXO inhibits the development of the long-winged morph by suppressing vestigial (Vg) expression during the wing-morph decision-making stage (Zhang et al., 2021). It appears that FOXO and REPTOR2, respectively, relay the insulin and TOR signaling cascades to control wing dimorphism in planthoppers and aphids. Alternatively, the BRLZ domain is required to form REPTOR/REPTOR-BP homo/hetero-dimer complex which conveys negative regulation of TOR signaling on genes related to autophagy (Tiebe et al., 2015). Our results are consistent with the canonical pathway regulated by TOR in that either knockdown of REPTOR2 or activation of TOR could attenuate autophagy in the wing disc. These results suggest that REPTOR2 from pea aphids served as a transcription factor to exert a negative effect on TOR-regulated autophagy initiation.

Insulin signaling is known to determine the wing-morph switch in planthoppers (Xu et al., 2015) and is also responsible for production of winged offspring regulated by miR-9b-ABCG4 cascade in brown citrus aphid (Shang et al., 2020). Furthermore, insulin could enhance TOR signaling by releasing the negative feedback of Akt on the tuberous sclerosis proteins TSC1 (hamartin) and TSC2 (tuberin) (Blagosklonny et al., 2009). It has been shown that embryos derived from pea aphids subjected to crowding treatment have higher insulin signaling (Grantham et al., 2019). This may lead to stronger TOR signaling in the first instar offspring, which could suppress wing disc autophagy and increase the proportion of winged aphids.

Gene duplication is a major source for novel gene production (Kaessmann, 2010; Prince and Pickett, 2002), which has become an important mechanism regulating phenotypic plasticity (Chen et al., 2013), including manipulating wing polyphenism in insects. For instance, a duplicated fs3 (follistatin 3) determined the wingless morph formation for male pea aphids (Li et al., 2020). Another duplicated gene InR2 (insulin receptor 2) was highly expressed in the wing bud of the planthopper that served as a regulatory switch of short-winged morph formation (Xu et al., 2015). Similarly, different from other seven aphid species with single copies of REPTOR, pea aphids possess two REPTOR genes. Although it has lost 2 exons, ApREPTOR2 has higher similarity in coding sequence with ApREPTOR1, but shares little similarity in the flanking regions. This is in agreement with the chromosomal distribution results indicating that ApREPTOR1 is located in A1 chromosome while ApREPTOR2 is in X chromosome. ApREPTOR2 is likely a duplicate from ApREPTOR1, followed by translocating from A1 to X chromosome. This may also warrant the reproductive role of sexual female in pea aphids because most sexual females are monomorphic wingless, whereas males that contain just single X chromosome are dimorphic (Brisson, 2010).

In the aphid wing polyphenism, differential expression of diverged paralogous genes could represent an adaptive response to particular environmental challenges (Shigenobu et al., 2010; Brisson et al., 2010). Evidently, ApREPTOR2-regulated wing disc degradation is significant for the winged- versus wingless-destined aphids, whereas the expression of its paralog ApREPTOR1 was unaffected by wing morphs or tissue types (Figure 3—figure supplement 1A). Knockdown of ApREPTOR1 did not affect the expression of ApREPTOR2 and ATGs and the proportion of winged aphids (Figure 3—figure supplement 1B–E). These results indicated that ApREPTOR2 rather than the canonical REPTOR activated a tissue-specific degradation in the wing disc and not a systemic PCD. Apparently, more research is necessary to further elucidate how other aphid species that contain a single REPTOR regulate autophagic degradation in the wing disc.

Sequencing data have been deposited in SRA under accession ID PRJNA857589.

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Author details

1. Erliang Yuan

   1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
   2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Science, Beijing, China

   Contribution

   Conceptualization, Data curation, Writing – original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7825-1908

2. Huijuan Guo

   1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
   2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Science, Beijing, China

   Contribution

   Formal analysis, Funding acquisition, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4432-6446

3. Weiyao Chen

   1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
   2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Science, Beijing, China

   Contribution

   Methodology

   Competing interests

   No competing interests declared

4. Bingru Du

   School of Life Science, Hebei University, Baoding, China

   Contribution

   Investigation

   Competing interests

   No competing interests declared

5. Yingjie Mi

   State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

   Contribution

   Methodology

   Competing interests

   No competing interests declared

6. Zhaorui Qi

   School of Life Science, Hebei University, Baoding, China

   Contribution

   Investigation

   Competing interests

   No competing interests declared

7. Yiyang Yuan

   Institute of Plant Protection, Shandong Academy of Agriculture Sciences, Jinan, China

   Contribution

   Data curation, Funding acquisition

   Competing interests

   No competing interests declared

8. Keyan Zhu-Salzman

   Department of Entomology, Texas A&M University, College Station, United States

   Contribution

   Writing – review and editing

   Competing interests

   No competing interests declared

9. Feng Ge

   Institute of Plant Protection, Shandong Academy of Agriculture Sciences, Jinan, China

   Contribution

   Supervision, Writing – review and editing

   For correspondence

   gef@ioz.ac.cn

   Competing interests

   No competing interests declared

10. Yucheng Sun

    1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Science, Beijing, China

    Contribution

    Conceptualization, Resources, Supervision, Funding acquisition, Project administration, Writing – review and editing

    For correspondence

    sunyc@ioz.ac.cn

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-2353-0218

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