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

Jana Křemenová,Christian Massino,Tomáš Bartonička,Oliver Otti,Klaus Reinhardt,Ondřej Balvín,Markéta Sasínková,Alfons R Weig

doi:10.1038/s41598-021-94622-6

Jana Křemenová, Christian Massino + Show 6 more

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https://doi.org/10.1038/s41598-021-94622-6

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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.

Highlights

Speciation proceeds if reproductive isolation is based on genetic differences[1,2]
If sperm performance adapts locally, reproductive isolation may occur, such as that observed in male fruit fly fertility associated with temperature[21] or different sperm motility in the substrate in mouthbrooding cichlid fish[22]
human lineage (HL) males induced more fertilised eggs when they are reared on a foreign diet than on their original diet, while bat lineage (BL) males induced similar numbers of fertilised eggs on either diet (Table 1a, Fig. 1a)

Summary

Introduction

Speciation proceeds if reproductive isolation is based on genetic differences[1,2]. A key question in speciation is whether the reproductive barrier arises first, reduces gene flow, and so drives populations and their ecological traits apart, i.e. reproductive isolation is a by-product of d ivergence[1] or whether divergent natural selection on specific traits exists that act as direct reproductive barriers (ecological s peciation[2]). The key male fitness parameter is sperm performance, in either isolation or in competition. This significance is reflected by the existence of hundreds of studies on sperm competition[3,4,5] and likely thousands of medical studies examining sperm (dys)function. Medical and evolutionary studies agree that environmental or lifestyle factors are responsible for a large part of the variation observed in sperm p erformance[7,9]. Sperm performance can evolve in response to the environment or respond plastically This distinction is important for evolutionary research because if sperm performance is plastic, gene flow between ecologically separated populations is not hampered. A protein-deficient diet can reduce sperm motility, count and viability, fertility rate, sperm mitochondrial activity, or hyaluronidase a ctivity[31,32,34]

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