Male diet affects female fitness and sperm competition in human- and bat-associated lineages of the common bedbug, Cimex lectularius

Abstract

Sperm performance can vary in ecologically divergent populations, but it is often not clear whether the environment per se or genomic differences arising from divergent selection cause the difference. One powerful and easily manipulated environmental effect is diet. Populations of bedbugs (Cimex lectularius) naturally feed either on bat or human blood. These are diverging genetically into a bat-associated and a human-associated lineage. To measure how male diet affects sperm performance, we kept males of two HL and BL populations each on either their own or the foreign diet. Then we investigated male reproductive success in a single mating and sperm competition context. We found that male diet affected female fecundity and changed the outcome of sperm competition, at least in the human lineage. However, this influence of diet on sperm performance was moulded by an interaction. Bat blood generally had a beneficial effect on sperm competitiveness and seemed to be a better food source in both lineages. Few studies have examined the effects of male diet on sperm performance generally, and sperm competition specifically. Our results reinforce the importance to consider the environment in which sperm are produced. In the absence of gene flow, such differences may increase reproductive isolation. In the presence of gene flow, however, the generally better sperm performance after consuming bat blood suggests that the diet is likely to homogenise rather than isolate populations.

Changes in body size and fertility due to artificial and natural feeding of laboratory common bed bugs (Heteroptera: Cimicidae)

“…Their lipid composition, however, has been shown to differ (Křemenová 2020) and bat blood is known to have about twice as many red blood cells as human blood (Jürgens et al 1981). Since bat blood was also shown to increase sperm competitiveness (Křemenová et al 2021), it is more likely to be beneficial for bed bugs, at least for BL, compared to human blood. The lower fertility of BL on the original blood source thus rather suggests that it may be difficult to reach regular optimal performance in laboratory feeding on bats.…”

“…The most common use of such colonies is testing insecticide susceptibility (Romero et al 2010, How and Lee 2011, Hardstone et al 2015), traps (Anderson et al 2009, Wang et al 2009), and more recently, training bed bug detection dogs (Pfiester et al 2008, Cannon et al 2020). In terms of basic research, the common bed bug ( Cimex lectularius ) is studied for genetic diversification between 2 naturally occurring host lineages, i.e., human-associated (HL) and bat-associated (BL) lineage (Balvín et al 2012, Booth et al 2015) and reproductive compatibility of the lineages addressing possible incipient sympatric speciation (Wawrocka et al 2015, Křemenová et al 2021). Further interests encompass rather general questions like traumatic insemination (Stutt and Siva-Jothy 2001, Reinhardt et al 2003), sperm metabolism (Massino et al 2022), reproductive immunity and sexually transmitted infections (Bellinvia et al 2020, Bellinvia et al 2020a, Thongprem et al 2020), the relationship with a primary symbiont, the Wolbachia bacteria (Hosokawa et al 2010, Balvín et al 2018), heteroplasmy (Robison et al 2015) or insecticide resistance-associated mutations (Dang et al 2015).…”

Effects of Wolbachia elimination and B-vitamin supplementation on bed bug development and reproduction

“…Furthermore, it remains to be determined whether dramatic effects on fecundity and hatch rate due to Wb elimination, are due exclusively to an effect on females, or whether reproduction is also affected in aposymbiotic males. It has been shown that the blood source fed to males can affect sperm competition and female fecundity 32 but the effect of Wb removal on male reproductive fitness has not been investigated. Both sexes house Wb in gonad-associated bacteriomes 16 , so the elimination of Wb might uniquely affect reproductive traits in females and males.…”

Effects of Wolbachia elimination and B-vitamin supplementation on bed bug development and reproduction

“…Furthermore, it remains to be determined whether dramatic effects on fecundity and hatch rate due to Wb elimination, are due exclusively to an effect on females, or whether reproduction is also affected in aposymbiotic males. It has been shown that the blood source fed to males can affect sperm competition and female fecundity 31 but the effect of Wolbachia removal on male reproductive tness has not been investigated. Both sexes house Wb in gonad-associated bacteriomes 16 , so the elimination of Wb might uniquely affect reproductive traits in females and males.…”