Mating-Induced Trade-Offs upon Egg Production versus Fertilization and Offspring’s Survival in a Sawfly with Facultative Parthenogenesis

Abstract

Investigation of mating-induced trade-offs between reproduction and survival is conducive to provide evolutionary insights into reproductive strategies and aging. Here, we used RNAseq and bioinformatics to reveal mating-induced changes of genes and pathways related to reproduction and survival in female Cephalcia chuxiongica, a pine defoliator with facultative parthenogenesis and long larval dormancy. Results showed that mating induced substantial downregulation on genes and pathways associated to immunity, stress response, and longevity. However, mating induced divergent reproductive response, with downregulation on genes and pathways related to egg production while upregulation on genes and pathways related to egg fertilization. Considering the nature of limited resources in adults, low fecundity, and egg protection behavior in C. chuxiongica, we suggest that mating triggers trade-offs between reproduction and survival in this insect and females of this species may have evolved specific strategies to adapt to the environmental and hosts’ conditions, e.g., restrict whole fecundity to ensure higher fertilization and offspring’s survival. Moreover, mating induced significant responses on genes and pathways that play important roles in vertebrate reproduction while their function in insects are unclear, such as the progesterone-mediated oocyte maturation pathway; the significant regulation after mating suggests that their function may be evolutionarily conserved in animal kingdom.

Mating-Induced Common and Sex-Specific Behavioral, Transcriptional Changes in the Moth Fall Armyworm (Spodoptera frugiperda, Noctuidae, Lepidoptera) in Laboratory

“…Previous studies generally found that mating induces the upregulation of egg production and fertilization rate [ 32 , 35 , 36 , 41 ], whereas in C. chuxiongica, mating induced divergent reproductive response, with downregulation on genes related to egg production, while upregulation on genes related to egg fertilization [ 38 ]. In the present study, functional enrichment analysis in S. frugiperda females showed there is more reproduction related terms/pathways enriched to upregulated DEGs than to downregulated DEGs (10:1) at 0 h postmating, which is less (1:14) at 6 h postmating, and then more (16:0) again at 24 h postmating.…”

“…Previous studies have shown that mating may also promote trade-offs between reproduction and survival, with increased reproductive activities after mating being likely to incur cost on soma maintenance [ 36 , 37 , 38 , 41 ]. In the present study, however, mating induced upregulation on response (such as response to external biotic stimulus, response to bacterium and response to external stimulus; Tables S8–S11 ) and soma maintenance (such as immune activity, stress reaction and detoxification; Tables S8–S11 ) related processes in S. frugiperda females at 0, 6 and 24 h postmating ( Figure 5 a–c).…”

“…Studies in Drosophila [ 32 , 33 , 34 , 35 ] and other insect species [ 36 , 37 , 38 ] demonstrated that mating can cause significant transcriptional changes in females [ 32 , 33 , 34 , 35 ], which may support them to obtain a high rate of fertilization and fecundity. These studies on different insect species, based on depth sequencing and bioinformatics, have provided further insights in this field.…”

Post-Mating Responses in Insects Induced by Seminal Fluid Proteins and Octopamine

“…Similar observations have been made in female Cephalcia chuxiongica, where reproductive-related genes are upregulated from 1 to 24 h after mating, while immune genes remain downregulated. After 24 h post-mating, longevity-related genes start to decline [102]. It is worth mentioning that the expression of female immune genes after mating shows species-specific, and even interspecies-specific, differences [103].…”