Initiation of flight muscle apoptosis and wing casting in the red imported fire ant Solenopsis invicta

Abstract

Newly‐mated Solenopsis invicta flight queens cast (shed) their wings within 24 h. An examination of their flight muscle cells reveals numerous apoptotic (terminal deoxynucleotidyl transferase mediated dUTP nick end labelling positive) nuclei. By contrast, flight muscle cells of mature alate virgin (MAV) females removed 24 h earlier from a managed laboratory colony exhibit neither wing casting nor the presence of apoptotic nuclei. Using MAV‐females, the initiation of flight muscle apoptosis and wing casting is compared with artificial mating using seminal fluid with sperm, seminal fluid with no sperm, saline as a negative control, the mating flight as simulated in the laboratory, elevated CO2 exposure, application of methoprene (a juvenile hormone analogue), or injection of 20‐hydroxyecdysone. Numerous apoptotic nuclei are revealed in the flight muscle cells of mated dealate females 24 h after a natural mating flight but not in MAV‐females controls. Only artificial mating of MAV‐females reveals a similar pattern of apoptotic nuclei flight muscle 24 h after insemination. None of the other factors tested induces flight muscle cell apoptosis in MAV‐females. Methoprene dissolved in methyl ethyl ketone, at a concentration of 0.44 ng per μL per ant, stimulates 90% of MAV‐females to shed their wings within 24 h, as opposed to 10% or less wing shedding for the methyl ethyl ketone control and all other treatments.

Oocyte membrane localization of vitellogenin receptor coincides with queen flying age, and receptor silencing by RNAi disrupts egg formation in fire ant virgin queens

“…This result implies that successful insemination of newly mated queens, but not flight only, triggers queen reproduction. In addition, the factors linked to this activation might not be involved in de‐alation [51]. In Drosophila , the sex peptide (transported from male to female when mating) and its receptor are essential for triggering the post‐mating reproductive switch [52,53].…”

Trade‐off between flight capability and reproduction in Acridoidea (Insecta: Orthoptera)

“…The long-winged grasshoppers invested a lot of energy for their flight muscles and short-winged and wingless species devoted more resources to gonad development. This trade-off also existed in many insect groups (Azizi et al, 2009;Castaneda et al, 2010;Chaudhuri, 2012;Conroy et al, 2018;Denno et al, 1989;Dingle, 2006;Elliott & Evenden, 2012;Guerra, 2011;Kaitala & Huldn, 1990;Khuhro et al, 2014;Steenman et al, 2014;Tigreros & Davidowitz, 2019;Wilson et al, 2020;Zhang et al, 2021). In addition, the trade-off between flight capability and reproduction is well known in crickets (Conroy et al, 2018;Guerra & Pollack, 2007;Mole & Zera, 1994;Nanoth Vellichirammal et al, 2014;Zeng & Zhu, 2012;Zera, 2003Zera, , 2016Zera & Brink, 2000;Zhao et al, 2016).…”

Biochemical, molecular, and morphological variations of flight muscles before and after dispersal flight in a eusocial termite, Reticulitermes chinensis

“…Muscular histolysis can: (i) avoid high maintenance costs of the flight muscles; and (ii) reallocate energy and nutrition from degenerating flight muscles to developing oocytes, both of which facilitate subsequent fecundity (Zera & Denno, 1997; Marden, 2000). In another eusocial hymenopteran, imported fire ants, the flight muscular histolysis in dealates has been observed to be initiated by apoptosis within 2 h of mating and has been correlated with increased sarcoplasmic calcium‐initiated muscle degradation via the ATP/ubiquitin‐dependent proteolytic pathway (Jones et al ., 1982; Azizi et al ., 2009). Furthermore, the flight muscle histolysis has been reported after dealation in crickets, or after migratory flight in alate aphids with simultaneously stimulated reproduction, which results from JH‐triggered programmed cell death (ubiquitin‐dependent apoptosis) (Kobayashi & Ishikawa, 1994; Tanaka, 1994; Oliver et al ., 2007; Yu et al ., 2020).…”

“…Therefore, the gradual degeneration/histolysis of flight muscles in size and internal myofibril and mitochondrial structure observed in R. chinensis after dispersal flight may be the result of ubiquitin‐dependent apoptosis, which is triggered by JH and may be accompanied with the transfer of nutrients from flight muscles to ovaries to enhance consequent reproduction, which has been indicated in Hodotermes mossambicus (Van der Westhuizen et al ., 1987). However, the degeneration of thoracic muscles after dispersal flight and consequent dealation in R. chinensis , which sustains for more than 33 d, is much slower than the muscular histolysis in other insects, especially in fire ants with muscular histolysis as early as 4–6 h after dispersal flight and consequent mating (Azizi et al ., 2009). The reason for this different time‐course is uncertain.…”

“…After flight, the wingless dealates of the termites concentrate on their pairing, mating and fecundity for the formation of a new colony, accompanied by the degeneration of the flight muscle to satisfy nutrient requirements (Johnson, 1969), which might result in morphological and functional changes in both the flight muscles, and the mitochondria therein. Similar phenomena of this fitness trade‐off between flight capability and reproduction (or flight‐oogenesis syndrome) have been reported in some wing‐polymorphic insects, such as ants, crickets, aphids, planthoppers, firebugs and water striders (Denno et al ., 1989; Kaitala & Huldén, 1990; Kobayashi & Ishikawa, 1994; Zera & Denno, 1997; Marden, 2000; Peeters & Ito, 2001; Socha & Šula, 2006; Azizi et al ., 2009; Heidinger et al ., 2018). For the negative association (trade‐off) between flight ability and fecundity, the mass, color, respiration, and enzyme activities of flight muscles have been found to differ between the macropters and brachypters of crickets (Zera et al ., 1999).…”