Male Seminal Fluid Substances Affect Sperm Competition Success and Female Reproductive Behavior in a Seed Beetle

Yamada, Takashi; Goenaga, Julieta; Rönn, Johanna Liljestrand; Arnqvist, Göran

doi:10.1371/journal.pone.0123770

Cited by 82 publications

(90 citation statements)

References 56 publications

(51 reference statements)

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“…Previous work on Tribolium beetles further suggests that the same proteins that promote fecundity stimulation might also reduce egg fertilisation success (Yamane et al. ). This could explain why we found Small burying beetle males to be both better at fecundity stimulation and to have relatively low P 2 scores.…”

Section: Discussionmentioning

confidence: 99%

Superior stimulation of female fecundity by subordinate males provides a mechanism for telegony

Pascoal

Jarrett

Evans³

et al. 2018

Evolution Letters

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When females mate promiscuously, rival males compete to fertilise the ova. In theory, a male can increase his success at siring offspring by inducing the female to lay more eggs, as well as by producing more competitive sperm. Here we report that the evolutionary consequences of fecundity stimulation extend beyond rival males, by experimentally uncovering effects on offspring. With experiments on the burying beetle Nicrophorus vespilloides, we show that smaller subordinate males are better able to stimulate female fecundity than larger, dominant males. Furthermore dominant males also benefit from the greater fecundity induced by smaller males, and so gain from the female's earlier promiscuity ‐ just as predicted by theory. By inducing females to produce more offspring on a limited resource, smaller males cause each larva to be smaller, even those they do not sire themselves. Fecundity stimulation thus promotes the non‐genetic inheritance of offspring body size, and provides a mechanism for telegony.

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Section: Discussionmentioning

confidence: 99%

Superior stimulation of female fecundity by subordinate males provides a mechanism for telegony

Pascoal

Jarrett

Evans³

et al. 2018

Evolution Letters

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“…These spines increase the passage of seminal fluid substances into the body of mated females (Hotzy et al ., ), suggesting an important role for the proteins within the seminal fluid of this species. Indeed, injecting females directly with SFPs alters female receptivity and male success in sperm competition (Yamane et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Novel seminal fluid proteins in the seed beetle Callosobruchus maculatus identified by a proteomic and transcriptomic approach

Bayram

Sayadi

Goenaga

et al. 2016

Insect Molecular Biology

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The seed beetle Callosobruchus maculatus is a significant agricultural pest and increasingly studied model of sexual conflict. Males possess genital spines that increase the transfer of seminal fluid proteins (SFPs) into the female body. As SFPs alter female behaviour and physiology, they are likely to modulate reproduction and sexual conflict in this species. Here, we identified SFPs using proteomics combined with a de novo transcriptome. A prior 2D-sodium dodecyl sulphate polyacrylamide gel electrophoresis analysis identified male accessory gland protein spots that were probably transferred to the female at mating. Proteomic analysis of these spots identified 98 proteins, a majority of which were also present within ejaculates collected from females. Standard annotation workflows revealed common functional groups for SFPs, including proteases and metabolic proteins. Transcriptomic analysis found 84 transcripts differentially expressed between the sexes. Notably, genes encoding 15 proteins were highly expressed in male abdomens and only negligibly expressed within females. Most of these sequences corresponded to 'unknown' proteins (nine of 15) and may represent rapidly evolving SFPs novel to seed beetles. Our combined analyses highlight 44 proteins for which there is strong evidence that they are SFPs. These results can inform further investigation, to better understand the molecular mechanisms of sexual conflict in seed beetles.

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“…1995). Whilst such a comprehensive analysis of female mating responses in seed beetles is yet to be undertaken, SFPs injected into females alter egg laying rate, female remating rate and male competitive fertilization success (Yamane et al 2015). These phenotypes likely result from postmating changes in expression of hundreds to thousands of genes in females in both reproductive and somatic tissues (Lawniczak and Begun 2004; McGraw et al.…”

Section: Introductionmentioning

confidence: 99%

Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

Immonen

Sayadi

Bayram

et al. 2017

Genome Biology and Evolution

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Sexually dimorphic phenotypes arise largely from sex-specific gene expression, which has mainly been characterized in sexually naïve adults. However, we expect sexual dimorphism in transcription to be dynamic and dependent on factors such as reproductive status. Mating induces many behavioral and physiological changes distinct to each sex and is therefore expected to activate regulatory changes in many sex-biased genes. Here, we first characterized sexual dimorphism in gene expression in Callosobruchus maculatus seed beetles. We then examined how females and males respond to mating and how it affects sex-biased expression, both in sex-limited (abdomen) and sex-shared (head and thorax) tissues. Mating responses were largely sex-specific and, as expected, females showed more genes responding compared with males (∼2,000 vs. ∼300 genes in the abdomen, ∼500 vs. ∼400 in the head and thorax, respectively). Of the sex-biased genes present in virgins, 16% (1,041 genes) in the abdomen and 17% (243 genes) in the head and thorax altered their relative expression between the sexes as a result of mating. Sex-bias status changed in 2% of the genes in the abdomen and 4% in the head and thorax following mating. Mating responses involved de-feminization of females and, to a lesser extent, de-masculinization of males relative to their virgin state: mating decreased rather than increased dimorphic expression of sex-biased genes. The fact that regulatory changes of both types of sex-biased genes occurred in both sexes suggests that male- and female-specific selection is not restricted to male- and female-biased genes, respectively, as is sometimes assumed.

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Male Seminal Fluid Substances Affect Sperm Competition Success and Female Reproductive Behavior in a Seed Beetle

Cited by 82 publications

References 56 publications

Superior stimulation of female fecundity by subordinate males provides a mechanism for telegony

Superior stimulation of female fecundity by subordinate males provides a mechanism for telegony

Novel seminal fluid proteins in the seed beetle Callosobruchus maculatus identified by a proteomic and transcriptomic approach

Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

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