Cryptic Female Choice and Other Types of Post-Copulatory Sexual Selection

Alfredo V. Peretti · Anita Aisenberg Editors Cryptic Female Choice in Arthropods Patterns, Mechanisms and Prospects Cryptic Female Choice in Arthropods A mating pair of syrphid flies. Photo Carlos Toscano-Gadea Alfredo V. Peretti · Anita Aisenberg Editors Cryptic Female Choice in Arthropods Patterns, Mechanisms and Prospects 1 3 Editors Alfredo V. Peretti Anita Aisenberg Instituto de Diversidad y Ecología Animal Laboratorio de Etología, Ecología y CONICET—Universidad Nacional de Evolución Córdoba Instituto de Investigaciones Biológicas Cordoba Clemente Estable Argentina Montevideo Uruguay ISBN 978-3-319-17893-6 ISBN 978-3-319-17894-3 (eBook) DOI 10.1007/978-3-319-17894-3 Library of Congress Control Number: 2015937214 Springer Cham Heidelberg New York Dordrecht London © Springer International Publishing Switzerland 2015 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. Printed on acid-free paper Springer International Publishing AG Switzerland is part of Springer Science+Business Media (www.springer.com) Foreword Cryptic Female Choice: A Tale About a Boy Who Loved Flies More than 30 years ago, I first presented the term “cryptic female choice” as a label for certain behaviors I discovered in female Harpobittacus nigriceps, a species of hangingfly (Mecoptera) (Thornhill 1983). Since then, cryptic female choice (CFC) theory has diversified and expanded, and in the process, so too have the hypotheses, concepts, and topics that comprise the broader field of sexual selection research. Traditionally, the process of sexual selection was restricted to variation among conspecific males in their mating success and associated reproductive success resulting from the males’ trait differences affecting competition for mates or being chosen as a mate by the opposite sex. This is the Darwinian or classical view of sexual selection in evolutionary biology. Parker’s (1970) ideas about sperm competition expanded this classical perspective to include sexual selection favoring male traits that solve the adaptive problem of a mate’s insemination by a sexual competitor and the resultant competition between ejaculates of different males for the egg(s) of a single female. The boundaries of sexual selection research were expanded again when Hrdy (1977) recognized that male infanticidal behavior toward offspring still under maternal care and sired by another male can increase the mating success of infanticidal males and hence cause sexual selection to act on males. CFC theory expanded Darwinian intersexual selection theory by recognizing that female choice could take place after mating started, too. CFC theory gives female choice a larger role in sexual selection and the evolution of male traits and mating systems. Cryptic choice by females extends female control in decisions affecting male reproductive success beyond the premating context and through all stages of the reproductive process. CFC traits cause variation in male reproductive success by their expression after mating starts, and CFC can continue to cause sexual selection on males during egg or offspring production by a female, and even after eggs are laid or offspring are born, if females differentially invest based on v vi Foreword the traits of the sires of their offspring. At the beginning of the discussion of CFC in insects in the literature, CFC was based on evolved adaptations of females that function to choose high-quality sires for offspring and/or defend against sexual coercion by males that circumvent female choice. Sire quality was discussed as male traits that increase mating success of sires’ sons and/or the fitness of both sexes of sires’ offspring (Thornhill 1983; Thornhill and Alcock 1983). The most compelling argument for the process of CFC (as well as Darwinian female choice) arises from Trivers (1972) insights about parental investment and sexual selection. As he emphasized, parental investment is any investment by a parent in an offspring that improves offspring survival and hence offspring reproductive success at the expense of the parent’s ability to invest in other offspring. Parental investment in a given generation then fundamentally causes the number and survival of offspring in the next generation and therefore becomes the focus of sexual/mating competition by the opposite sex. Males compete with other males to capture the parental investment of females that can be obtained through sir- ing eggs. Females, by contrast, as the sex that typically has the largest obligate parental investment, have adaptations that function to adaptively allocate their limited parental investment through tight control of that investment and its efficient expenditure. Females are hence designed to assess ecological circumstances that affect efficient expenditure of their parental investment and to differentially allocate parental investment depending on how circumstances affect its adaptive use. These decisions are designed to be sensitive to variation in conditions that affect optimal allocation of parental investment and hence the reproductive profits females receive from their investments. Sire and mate quality is one such condi- tion that is widely important. Hence, females are selected to assess the quality of their mates and the sires of their offspring and bias investment toward high quality ones. It is often maladaptive for females that this assessment and related investment allocation process end when mating begins. Maximum female reproductive success is typically dependent upon females continuing their control of the relative success of different mates subsequent to the premating context and for females to extend their influence over which mate and sire receives their limited parental investment. In particular, females gain in reproductive success by extending this control of the paternity of offspring when (a) females engage in what John Alcock and I called convenience polyandry in which females adaptively mate with multi- ple males to reduce the costs of rejecting them (Thornhill and Alcock 1983); (b) circumstances prevent the female’s full assessment of male quality before mating; (c) males circumvent female choice by sexual coercion; or (d) females can obtain non-genetic material benefits from males (e.g., nuptial gifts) by mating with mul- tiple males. About a decade after publication of my paper on CFC, Eberhard (1996) made a strong case for the importance of CFC in Female Control: Sexual Selection by Cryptic Female Choice by reviewing much of the evidence at the time in favor of CFC and detailing many mechanisms by which it may occur. Arnqvist (2014) recently analyzed the historical trend in scientific papers that contain “cryptic female choice” since the term first appeared in 1983. The published research Foreword vii referencing the term was almost nil before the mid-1990s and then began a steady climb that is still seen; this trend is due fundamentally to Bill Eberhard’s book which has promoted many new avenues of CFC research and had significant scientific impact. Researchers in a broad range of circumstances and studying diverse animal taxa have published evidence for CFC, and the current collection of book chapters treats that research across arthropods and offers many new findings and research directions. Darwin did not live to see the heuristic success of his theory that female choice played an important role in the evolution of male traits. Female choice was per- haps Darwin’s most controversial theory in his entire treatment of life’s history as evolutionary history (Bajema 1984). Darwin held fast to his ideas about the important role of female choice in evolution up to his death. His last defense of the evolutionary perspective was a defense of female choice and was read to the public at a meeting of the Zoological Society of London just hours before he died (Bajema 1984, p. 150). No doubt Darwin would be thrilled to know of the many hundreds of empirical documentations of female premating choice and male adaptations that function to impress females in many taxa that followed the explosion of sexual selection research beginning in the early 1970s and continuing today. And no doubt he would be thrilled to know his nascent insights about female choice were even more powerful and far-reaching than he recognized, which is seen in the evidence for CFC. I suspect this collection of chapters on CFC in arthropods would greatly impress Darwin and be among his favorite books. To be asked to write the forward

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