Differential immune-gene expression in sperm storage organs of leaf-cutting ants

Abstract

Leaf-cutting ant queens mate with multiple males during a single nuptial flight and store sperm for up to two decades. During mating, males transfer sperm from their accessory testes to the queen bursa copulatrix from where it enters the spermatheca, an insect sperm storage organ that has become highly specialized in long-lived ant queens who never re-mate later in life. Long-term storage without the possibility to obtain new sperm creates an immune defence dilemma, because recognition of non-self cells eliminates infections but may also target irreplaceable sperm and reduce lifetime reproductive success. We therefore hypothesized that non-specific immune responses, like pathogen melanization, should be silenced in the spermatheca, because they rely on general non-self recognition, and that specific responses such as antimicrobial peptides are activated instead as they specifically target pathogenic bacteria and/or fungi. The maintenance of uninfected sperm cells by males before mating is not constrained by non-self recognition, meaning immune regulation might be more liberal in male reproductive organs. To test this hypothesis, we measured gene expression of two antimicrobial peptides, abaecin and defensin, and prophenoloxidase, an important enzyme of the melanization pathway, in male accessory glands and testes and in queen bursae copulatrix and spermathecae of and leaf-cutting ants. As expected, prophenoloxidase expression was low in reproductive organs that sustain prolonged contact with sperm, whereas antimicrobial peptides showed average to high expression, indicating that leaf-cutting ants invest in specific rather than generalist immune defences for pathogen protection in organs that store sperm.

Molecular insights into post‐mating immune response in a fish with internal fertilization

“…These results, therefore, suggest a multifaceted response of the immune system in the female reproductive tract, rather than a general depression of its immune response. A mosaic‐like modulation of the immune response after ejaculate contact has been reported in other taxa, from insects (Chérasse, Baer, Schiøtt, & Boomsma, 2018) to mammals (Chavan et al, 2017).…”

“…Up‐ and down‐regulation of different components of the female immune response to mating has been found in Drosophila melanogaster , due to differential response to sperm or seminal fluid components (McGraw et al, 2004). Similarly, in ants, different components of the queen immune response are up‐ or down‐regulated in response to the ejaculate, suggesting that immune response after mating might be more precisely regulated than previously thought, with specific antimicrobial peptides over‐expressed to fight pathogens potentially transferred with the ejaculate, whereas other components of immunity instead are down‐regulated (Chérasse et al, 2018). The down‐regulation effect in guppy appears to be transitory as after 6 hr the genes related to immune response that were down‐regulated at 1h were expressed at a comparable level in C_6h and EJ_6h.…”

Effects of Mating on Gene Expression in Female Insects: Unifying the Field

“…Contrary to OBP25 that has the same pattern across insect species, the immune gene defensin has a different pattern of regulation in different species but it is regulated by mating in females of at least six species including Atta colombica (Hymenoptera: Formicidae), Ae. aegypti, C. capitata, D. melanogaster, L. niger and A. mellifera [23,29,34,58,62,63]. Like defensin, GDH that plays a role during insect metabolism has a different regulation pattern after mating in D. melanogaster, Ae.…”

“…For example, genes encoding the antimicrobial peptide (AMP), defensin, is upregulated after mating in Atta colombica, Ae. aegypti, B. dorsalis, Ceratitis capitata (Diptera: Tephritidae), D. melanogaster, Lasius niger (Hymenoptera: Formicidae) [23,25,29,58,62,63] whereas it is downregulated after mating in A. mellifera [34]. Within D. melanogaster, defensin (as well as other AMP genes) expression is lower in mated females relative to unmated females at 12 h post bacterial infection but higher at 24 h post-infection [63].…”

Hygienic behavior and antimicrobial peptide expression of the leaf-cutting ant Atta cephalotes (Hymenoptera, Formicidae) to Metharhizium anisopliae

“…Previously reported primers were used for abaecin and ribosomal protein L18 (rpL18) (Chérasse et al 2018). For the defensin and NADH dehydrogenase (NADH), primers were designed by Primer-BLAST (NCBI) using A. cephalotes-specific sequences available in the Gen Bank (NCBI) for defensin (BK008405.1) and NADH (XM_012205180.1).…”