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INBREEDING DEPRESSION in the GLANVILLE FRITILLARY BUTTERFLY (Melitaea Cinxia)

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INBREEDING DEPRESSION in the GLANVILLE FRITILLARY BUTTERFLY (Melitaea Cinxia) Department of Ecology and Systematics Division of Population Biology PO Box 65 (Viikinkaari 1) 00014 University of Helsinki Finland INBREEDING DEPRESSION IN THE GLANVILLE FRITILLARY BUTTERFLY (Melitaea cinxia) Sari Haikola Academic dissertation To be presented, with permission of the Faculty of Science of the University of Helsinki, for public criticism in the Auditorium 1041 of Viikki Biocentre 2 (Viikinkaari 5) on December 19th 2003 at 12 o‘clock noon. Helsinki 2003 © Kluwer Academic Publishers (I) © Finnish Zoological and Botanical Publishing Board (II) © authors (other parts) Cover photo by Tapio Gustafsson Author´s address: Department of Ecology and Systematics Division of Population Biology PO Box 65 (Viikinkaari 1) 00014 University of Helsinki Finland e-mail: [email protected] ISBN 952-91-6679-6 (Paperback) ISBN 952-10-1501-2 (PDF, http://ethesis.helsinki.fi) Yliopistopaino Helsinki 2003 3 INBREEDING DEPRESSION IN THE GLANVILLE FRITILLARY BUTTERFLY (MELITAEA CINXIA) Sari Haikola The thesis is based on the following articles or manuscripts: I Haikola, S., Fortelius, W., O‘Hara, R.B., Kuussaari, M., Wahlberg, N., Saccheri, I.J., Singer, M.C. and Hanski, I. 2001. Inbreeding depression and the maintenance of genetic load in Melitaea cinxia metapopulations. Conservation Genetics 2: 325–335. II Haikola, S. 2003. Effects of inbreeding in the Glanville fritillary butterfly (Melitaea cinxia). Annales Zoologici Fennici 40: 483–493. III Haikola, S. 2003. Effects of larval group size and host plant species on inbreeding depression in the Glanville fritillary butterfly. Manuscript. IV Haikola, S. and Sarhan, A. 2003. Parental similarity, heterozygosity and offspring fitness in the Glanville fritillary butterfly (Melitaea cinxia). Manuscript. V Haikola, S., Singer, M.C. and Pen, I. 2003. Has inbreeding depression led to avoidance of sib mating in the Glanville fritillary butterfly (Melitaea cinxia)? Submitted. These are referred to by their Roman numerals in the text. 4 CONTRIBUTIONS The following table shows the major contributions of authors to the original articles or manuscripts. I II III IV V Original idea IH SH SH IH, SH SH Study design IH, IS SH SH SH SH, MS Data gathering MK, WF, MS, SH SH SH, AS SH, MS, IP SH, NW Analyses SH,RO SH SH SH SH Manuscript SH SH SH AS, SH SH, MS preparation AS = Alia Sarhan, IH = Ilkka Hanski, IP = Ido Pen, IS = Ilik. J. Saccheri, MK = Mikko Kuussaari, MS = Michael C. Singer, NW = Niklas Wahlberg, RO = Robert B. O‘Hara, WF = Wilhelm Fortelius Supervised by Prof. Ilkka Hanski University of Helsinki FINLAND Reviewed by Jukka Jokela University of Oulu FINLAND Hanna Kokko University of Helsinki FINLAND Examined by Jouni Aspi University of Oulu FINLAND 5 CONTENTS 0 Summary Introduction 7 The study species 9 Overview of this thesis 10 Laboratory experiments 11 Results and discussion 13 Presence and severity of inbreeding depression in M. cinxia 13 Purging/maintenance of genetic load 14 The relationship between heterozygosity and parental relatedness, population connectivity and offspring fitness 14 No inbreeding avoidance 15 General discussion and conclusions 15 Acknowledgements 17 References 18 I Inbreeding depression and the maintenance of genetic load in Melitaea cinxia metapopulations Introduction Material and methods Laboratory experiments Mating success Experiment 1 Egg hatching rate Experiment 2 Experiment 3 Post-diapause survival Experiment 4 Statistical analyses Mating success Egg hatching rate Results Mating success Egg hatching rate Experiment 2 Experiment 3 Larval survival and growth Discussion Acknowledgements References II Effects of inbreeding in the Glanville fritillary butterfly (Melitaea cinxia) Introduction Material and methods Laboratory experiments 6 Statistical analyses The effect of the oviposition delay Comparison of the effects of inbreeding between the two generations The importance of the inbreeding history of the two sexes Results The effect of the oviposition delay Inbreeding depression in the two generations Discussion Acknowledgements References III Effects of larval group size and host plant species on inbreeding depression in the Glanville fritillary butterfly Introduction Material and methods Material 1 Material 2 Statistical analysis Results Discussion Acknowledgements References IV Parental similarity, heterozygosity and offspring fitness in the Glanville fritillary butterfly (Melitaea cinxia) Introduction Material and methods Study species Laboratory experiments Molecular methods Statistical analyses Results Discussion Acknowledgements References V Has inbreeding depression led to avoidance of sib mating in the Glanville fritillary butterfly (Melitaea cinxia)? Introduction Methods Laboratory experiments Field experiments Results Discussion Acknowledgements References Introduction 7 INTRODUCTION worth 1987). Both hypotheses are based on the fact that inbreeding increases ho- Ongoing habitat loss and fragmentation mozygosity. According to the partial have caused the extinction of innumera- dominance hypothesis, inbreeding de- ble natural populations and reduced the pression is due to the expression of dele- sizes of many others (Frankham 1995). terious recessive alleles in homozygous Small and isolated populations are at risk condition in inbred individuals. The to go extinct due to several demographic overdominance hypothesis suggests that and environmental factors. For example, inbreeding depression is attributable to the extinction risk of small local popula- overdominance, the heterozygote superi- tions of the Glanville fritillary butterfly ority over homozygous genotypes (Char- (Melitaea cinxia) in the Åland Islands in lesworth and Charlesworth 1987). These southwest Finland is affected by demo- two hypotheses differ in their predictions graphic and environmental stochasticity, for the effects of prolonged inbreeding. habitat loss, parasitism, emigration from The partial dominance hypothesis pre- small habitat patches and so forth dicts that the genetic load decreases dur- (Hanski 1998). Genetic factors are also ing continuous inbreeding due to selec- important in affecting the dynamics of tion purging deleterious recessive alleles small local populations of M. cinxia from the population. On the contrary, if (Saccheri et al. 1998). Evidently, these inbreeding depression were due to over- factors are not independent: for instance, dominance, the genetic load would not patch quality may affect population size, be reduced in later rounds of inbreeding which in turn affects the genetic proper- (except in the case of asymmetrical over- ties of the population. dominance, Barrett and Charlesworth Inbreeding, mating with close rela- 1991). The partial dominance hypothesis tives, is thought to have harmful effects has gained much support and is widely on general viability of individuals. The thought to explain most of the inbreed- reduced fitness of inbred individuals rel- ing depression that occurs in natural ative to more outbred ones is called in- populations (Charlesworth and Charles- breeding depression (Hedrick and Kali- worth 1987). nowski 2000). Traits that show inbreeding The existence and severity of inbreed- depression are often closely related to fit- ing depression in different organisms ness (Frankel and Soulé 1981, Falconer have been mainly studied in laboratory/ and MacKay 1996). Thus many life-his- captivity. The importance of inbreeding tory traits of a species may be adversely in captive populations of many species affected by inbreeding, whereas metric has been firmly established (see for ex- characters may not show any inbreeding ample Ralls and Ballou 1983, Ralls et al. depression. For example, Roff (1998) 1988, Dole and Ritland 1993). Ralls et al. found that inbreeding significantly de- (1988) examined the level of inbreeding creases fecundity in the sand cricket, depression in 40 captive mammalian Gryllus firmus, but morphological traits populations. The cost of close inbreeding such as egg length did not show any or on juvenile survival was very high, al- only very weak inbreeding depression. though the severity of inbreeding de- Similarly, the effects of inbreeding can pression varied greatly between popula- differ between early and late life-stages tions (Ralls et al. 1988). The role of (Husband and Schemske 1995). inbreeding depression in natural popula- There are two main hypotheses to tions is more difficult to assess (Pusey explain the occurrence of inbreeding de- and Wolf 1996). Traditionally, the level pression (Charlesworth and Charles- of inbreeding in a given population has 8 Introduction been determined directly using pedigree other studies such an effect was not information. With new molecular/genet- found (Dahlgaard and Loeschcke 1997, ic methods, the level of inbreeding in a Armbruster et al. 2000). In Drosophila population can also be assessed indirect- melanogaster inbreeding increases sus- ly using molecular markers (Box 1, see ceptibility to several stresses such as des- also for example Bensch et al. 1994, iccation (Dahlgaard and Hoffmann Amos et al. 2001). There are also prob- 2000). lems in assessing the level of inbreeding In theory, inbreeding depression from genetic data (Hansson and Wester- could be alleviated during repeated berg 2002), but the new techniques have rounds of inbreeding. The hypothesis of enabled researchers to study the effects continuous inbreeding purging the dele- of inbreeding in various species from terious recessive alleles from a popula- which it is not possible to obtain detailed tion
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