Frequent mating reduces male mating rate but not offspring quality or quantity in a neriid fly

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Frequent mating reduces male mating rate but not offspring quality or quantity in a neriid fly Erin L. Macartney1   · Russell Bonduriansky1 · Angela J. Crean2 Received: 4 March 2020 / Accepted: 1 September 2020 © Springer Nature Switzerland AG 2020

Abstract Frequent mating can deplete sperm and seminal fluid, limiting male ability to sire offspring. Frequent mating could also deplete non-genetic ejaculate components that affect offspring quality. These effects of frequent mating on male reproductive success may be mediated by male condition, or by modification of subsequent male mating behaviour. Using the neriid fly Telostylinus angusticollis, we conducted two experiments to examine whether a history of frequent mating affects males’ subsequent mating rate and offspring traits. The first experiment tested whether male condition (manipulated by varying larval diet quality) and mating history affects male performance in a subsequent mating with a single novel female whereby we predicted effects of previous mating may be more prevalent in low-condition males. Prior mating resulted in a reduction in mating rate with the novel female, but we did not detect an effect of mating history or male condition on offspring quality or quantity. The second experiment tested whether costs of mating become more evident when males encounter multiple novel females. Surprisingly, while prior mating once again resulted in a reduction in mating rate with the novel females, we still did not detect an effect of condition or mating history on any offspring traits. Therefore, male neriid flies appear to be able to mate many times without suffering a reduction in offspring quality or quantity. The apparent lack of an effect of frequent mating on such traits could be mediated by a reduction in mating rate, reflecting male prudence with ejaculate expenditure. Keywords  Sperm · Seminal fluid · Ejaculate depletion · Ejaculate allocation · Non-genetic · Paternal effects

Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1068​ 2-020-10076​-8) contains supplementary material, which is available to authorized users. * Erin L. Macartney [email protected] 1

Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, UNSW Sydney, Sydney, NSW, Australia

2

School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia



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Evolutionary Ecology

Introduction Frequent mating can deplete the male ejaculate and reduce the ability to sire offspring (e.g., Dewsbury 1982; Preston et al. 2001; Torres-Vila and Jennions 2005; Marcotte et al. 2007; Wigby et al. 2009; Reinhardt et al. 2011; Muller et al. 2016; Hopkins et al. 2019). For example, male Soay rams (Ovis aries) become sperm depleted over the course of the breeding season leading to a reduction in the number of lambs sired (Preston et al. 2001). This reduction in offspring quantity with mating can occur rapidly in some species. For example, three to five matings