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Mechanisms of Life History Evolution the Genetics and Physiology of Life History Traits and Trade-Offs OUP CORRECTED PROOF – FINAL, 04/23/2011, SPi Mechanisms of Life History Evolution The Genetics and Physiology of Life History Traits and Trade-Offs !"#$!" %& Thomas Flatt Group Leader at the Institute of Population Genetics at the Vetmeduni Vienna, Austria Andreas Heyland Assistant Professor at the Department of Integrative Biology at the University of Guelph, Canada 1 OUP CORRECTED PROOF – FINAL, 04/23/2011, SPi 3 Great Clarendon Street, Oxford ox2 6dp Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide in Oxford New York Auckland Cape Town Dar es Salaam Hong Kong Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto With offi ces in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries Published in the United States by Oxford University Press Inc., New York Oxford University Press 2011 The moral rights of the authors have been asserted Database right Oxford University Press (maker) First published 2011 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this book in any other binding or cover and you must impose the same condition on any acquirer British Library Cataloguing in Publication Data Data available Library of Congress Cataloging in Publication Data Library of Congress Control Number: 2011920657 Typeset by SPI Publisher Services, Pondicherry, India Printed in Great Britain on acid-free paper by CPI Antony Rowe, Chippenham, Wiltshire ISBN 978–0–19–956876–5 (Hbk.) 978–0–19–956877–2 (Pbk.) 1 3 5 7 9 10 8 6 4 2 OUP CORRECTED PROOF – FINAL, 04/23/2011, SPi CHAPTER 10 Mechanisms of nutrient-dependent reproduction in dipteran insects Alan O. Bergland environments affect genotypic performance by 10.1 Introduction altering life history traits then genetic variation Reproductive output, along with development time will likely be observed. and lifespan, are the core parameters of an organ- The persistence of genetic variation in life history ism’s life history. Together, these three parameters traits due to marginal overdominance is plausible allow us to predict an individual’s ! tness and, given the sensitivity of many life history traits to the by extrapolation, the growth rate of a population. environment ( Roff 2002 , Hodin 2009 ). In general, Ultimately, natural selection should act to maximize the three major environmental variables affecting ! tness ( Fisher 1930 ) and as a consequence these life life history traits are photoperiod, temperature, and history traits will respond in a correlated fashion nutrition. Photoperiod, at least for many organisms ( Robertson 1968 ). living in seasonal environments (e.g., Chapter 9 ), The study of life history traits has repeatedly plays a major role in determining the timing of demonstrated that they show reduced genetic development and reproduction (cf., Chapter 18 ). variation relative to putatively neutral characters For these species, alterations in the timing of life such as morphological traits ( Roff 2002 ). history transitions affect the length of the growing Presumably, reduced genetic variation in ! tness season and consequently the number of reproduc- components is due to the constant action of natu- tive cycles per year. In many organisms, notably ral selection to maximize ! tness. Although genetic ectothermic animals, exposure to variable tempera- variation in life history traits is generally low, it is tures affects development time, reproductive out- still present in many populations. The presence of put, and lifespan. This effect is mediated by changes genetic variation for life history traits is possibly in the rate of metabolic and catabolic processes that due to mutation–selection balance (discussed in are direct functions of temperature. Finally, nutri- Charlesworth and Hughes 2000 ), life history tion affects life history traits by altering the rate and trade-offs (see several chapters in Part 6 of this duration of larval growth and by directly limiting volume), or some form of balancing selection such resources available for reproduction and somatic as genetic overdominance or, more likely, environ- maintenance ( Chapter 11 ). The biology of nutrient- mentally dependent marginal overdominance dependent reproduction is reasonably well under- (e.g., Chapter 18 ). In this last scenario, environ- stood and is mediated by a complex set of mental variation affects life history traits but not interactions between molecular processes, mor- all genotypes are affected the same way. For phology, and intraspeci! c interactions. instance, one genotype may do very well in one The goal of this chapter is to integrate what is environment but very poorly in another; an alter- known about the molecular, morphological, and native genotype may have the opposite pattern. behavioral basis of one aspect of an organism’s life Such a scenario can lead to the stable persistence history: reproduction. In particular, I will focus of these two, hypothetical, genotypes. If these on recent developments that have been made in 127 OUP CORRECTED PROOF – FINAL, 04/23/2011, SPi 128 MECHANISMS OF LIFE HISTORY EVOLUTION understanding the mechanistic basis of nutrient-de- ulation and potentially invest fewer resources into pendent reproduction in dipteran insects. Although each female. Below, I discuss these four mechanisms I will be focusing on dipteran insects, it is reasonable in detail. to hypothesize that many of these mechanisms are shared among more divergent animals. 10.2.1 Ovary size This chapter will be divided into three main sec- tions. The ! rst section will examine the relationship The insect ovary is composed of repeated structures between larval nutrition and adult reproduction via called ovarioles (reviewed in Hodin 2009 ) and each growth and will focus on two related processes. ovariole is capable of simultaneously producing an First, I will discuss how nutrition affects the physi- egg. Therefore, given suf! cient adult nutrition, cal size of the adult and how body size and other ovariole number sets an upper limit on reproduc- allometric correlates directly relate to reproductive tive rate and capacity ( David 1970 ). capacity. Second, I will discuss how larval nutrition The positive relationship between ovariole provisions the adult with nutritive resources neces- number and fecundity is present within and sary for reproduction. amongst species of Diptera (reviewed in Honek In the second section of this chapter, I will focus 1993 ). For instance, variation in ovariole number on the relationship between adult nutrition and within populations of D. melanogaster is positively reproduction. In this section, I will cover the role of correlated with fecundity ( David 1970 , Bergland the sensory, digestive, and endocrine systems and and Tatar, unpublished data). Likewise, variation their role in reproduction. Finally, I will conclude in ovariole number amongst populations of the chapter by highlighting recent ! ndings that D. melanogaster is correlated with fecundity (e.g., integrate advances in the mechanistic basis of nutri- Boulétreau-Merle et al. 1982 ). Finally, variation ent-dependent reproduction with the predictions in ovariole number amongst closely related that evolutionary theory makes about the dynamics Drosopholids (reviewed in Hodin 2009 ) is posi- of life history evolution. tively correlated with fecundity. While there is abundant genetic variation in ovariole number, it is also highly sensitive to the 10.2 Larval nutrition and reproduction larval environment (e.g., reviewed in Hodin 2009 ) For Dipterans, larval nutrition affects female repro- and in particular to larval nutrition (e.g., Bergland duction by mediating various aspects of adult body et al. 2008 and references therein). Hodin and size. Environmentally induced variation in body Riddiford ( 2000 ) showed that for Drosophila mela- size and other allometric correlates affect fecundity nogaster larval nutrition affects ovariole number by through at least four mechanisms. First, larval nutri- modifying the rate of differentiation of a specialized tion affects ovary size, which is a direct determinant set of cells at the anterior tip of the ovariole—the of reproductive capacity. This effect appears to be terminal ! lament cells. Interestingly, this variable universal amongst Dipterans. Second, larvally rate of differentiation occurs during the wandering acquired nutrients are often necessary for adult stage, a period when larvae are no longer feeding. reproduction and thus the extent of larval nutrition This observation suggests that the ovariole number directly affects the number of eggs that can be pro- is set by endocrine or paracrine signals from another visioned. Third, adult body size is directly related tissue that is growing in direct response to larval to adult meal size in
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