Bottlenecks and Blowflies Speciation, Reproduction and Morphological Variation in Lucilia
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Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 660 _____________________________ _____________________________ Bottlenecks and Blowflies Speciation, Reproduction and Morphological Variation in Lucilia BY ANN-BRITT FLORIN ACTA UNIVERSITATIS UPSALIENSIS UPPSALA 2001 Dissertation for the Degree of Doctor of Philosophy in Animal Ecology presented at Uppsala University in 2001 Abstract Florin, A.-B. 2001. Bottlenecks and blowflies. Speciation, reproduction and morphological variation in Lucilia. Acta Universitatis Upsaliensis. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 660. 40 pp. Uppsala. ISBN 91- 554-5133-0. This thesis attempts to improve our understanding of the role of population size for the process of speciation. First, the effect of population size on speciation is studied using several meta-analyses of published laboratory experiments. Second, the effect of population size on behaviour is studied using a laboratory population of the blowfly Lucilia sericata. Third, the effect of population size on morphological and genetic variation is studied using wings and microsatellites from wild populations of L. illustris as well as experimentally bottlenecked populations of L. sericata. The meta-analyses showed that the result of many previous laboratory experiments on sympatric and parapatric speciation may have been biased by too small population sizes. Reduced interbreeding was less likely to develop in small populations where the selection against hybridisation often seemed to have been opposed by inbreeding depression or loss of genetic variation. In allopatric speciation experiments, no general consistent effect of population size was observed. There was no support for speciation through founder events. In fact, significant assortative mating was only found in vicariance experiments where derived populations was tested against each other. Population size influenced reproductive behaviour in L. sericata. There was a positive effect of increasing number of males on egg-laying but only as long as the female was in the company of at least one other female. Female mate choice and a positive effect of number of eggs on larval survival are suggested to be the underlying factors. No historic bottlenecks could be detected in the fly populations, but strong genetic indications suggest a fine grained genetic population structure of wild Lucilia flies. Bottlenecks had unpredictable effects on wing morphology as well as on genetic variation and fitness in a laboratory stock of L. sericata. Thus a bottlenecked population will not necessarily have a higher chance of evolving morphological novelties than one which has not undergone a bottleneck. However, among many bottlenecked populations there is a good chance that in at least one of them the conditions will be conducive to morphological change and evolution. In this statistical sense, thus, strong population fluctuations may enhance the probability of speciation events. Key words: Population size, speciation, Lucilia sericata, morphological variation, Lucilia illustris, bottlenecks. Ann-Britt Florin, Department of Animal Ecology, Evolutionary Biology Centre, Norbyv. 18D, SE-752 36 Uppsala, Sweden ([email protected]) © Ann-Britt Florin 2001 ISSN 1104-232X ISBN 91-554-5133-0 This thesis is based on the following papers, which will be referred to in the text by the roman numerals I-VI I Ödeen, A. & Florin, A.-B. 2000. Effective population size may limit the power of laboratory experiments to demonstrate sympatric and parapatric speciation. Proc. R. Soc. Lond. B. 267, 601-606. II Florin, A.-B. & Ödeen, A. Laboratory environments are not conducive for allopatric speciation. J. Evol. Biol. In press. III Florin, A.-B. Group size and composition affects reproduction in blowflies. Manuscript. IV Florin, A.-B. Morphological and genetic variation in wild populations of Lucilia illustris (Diptera: Calliphoridae). Manuscript. V Florin, A.-B. The effects of bottlenecks on morphological and genetic variation in Lucilia sericata (Diptera: Calliphoridae). Manuscript. VI Florin, A.-B. & Gyllenstrand, N. Isolation and characterization of polymorphic microsatellite markers in the blowflies Lucilia illustris and Lucilia sericata. Manuscript. Reprints were made by permission from the publisher. In paper I and II both authors contributed equally to the work. In paper VI the order of the authors reflects their involvement in the paper. Cover illustration and blowfly photo p. 7, copyright Mark C. Cassino. Contents INTRODUCTION 5 Speciation 5 The study species 7 GENERAL METHODS 9 Morphological data 9 Morphological integration 10 Genetic data 11 RESULTS AND DISCUSSION 12 Population size and sympatric and parapatric speciation 12 Population size and allopatric speciation 15 Population size and reproduction in blowflies 19 Genetic and morphological variation in wild L. illustris 21 Bottlenecks and morphological and genetic variation in L. sericata 24 CONCLUSIONS 28 ACKNOWLEDGEMENT 30 REFERENCES 30 SVENSK POPULÄRVETENSKAPLIG SAMMANFATTNING/ SWEDISH SUMMARY 38 4 INTRODUCTION Why are there so many species? This is a question that has been asked by mankind since the beginning of time. At the same time the preservation of form, morphologic stasis, is also apparent (Wake et al., 1983; Larson, 1989; Björklund, 1991, 1996; Benton & Pearson, 2001). Some traits differ greatly even in closely related species while other traits seem to stay unaltered through million of years (Gould & Eldredge, 1977; Turner, 1986). This paradox of stasis and yet a biological richness has led to the concepts of limiting adaptive gene complexes and founder effect which could break these complexes and allow for evolution of morphological novelties and even lead to speciation. Dobzhansky (1937) coined the term “coadaptation of the gene pool” meaning that the fitness of a gene is dependent on its genetic environment. Because genes are integrated, the adaptive value of a genotype is a property of the whole genome rather than of the constituent genes, and hence further evolution may require a thorough rebuilding of the genotype. Several lines of evidence suggest that such coadapted gene complexes exist (Cavener & Clegg, 1981; Carson & Templeton, 1984; Service & Rose, 1985; Stephan & Kirby, 1993; Clarke, 1997). Different models (peripatric speciation (Mayr, 1954); founder-flush speciation (Carson, 1975); accidental loss of male courtship behaviour (Kaneshiro, 1976); genetic transilience theory (Templeton, 1980); variance induced peak shifts (Whitlock, 1995)) offer alternative proposals how these complexes may break up and allow evolution to continue. Common for these models, however, are the stress on the stochastic effects of inbreeding and genetic drift associated with small population size. Speciation Mayr (1942) defines a species as a set of "groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups". I will use this Biological Species Concept throughout the thesis. Allopatric speciation, where new species arise from geographically isolated populations of the same ancestral species, is the most widely accepted of all current speciation models (Mayr, 1942, 1963; Lynch, 1989; Coyne, 1992; Rice & Hostert, 1993). It can be divided into vicariance and peripatric (or “peripheral isolates”) speciation (Lynch, 1989) depending on the location of the geographical split and the size of the sub- populations. In vicariance speciation (“the dumbbell model” in Mayr (1982)) a continuous population is split in the centre of its distribution, 5 giving rise to two or more large, isolated sub-populations. With time the sub-populations are thought to evolve reproductive isolation as a by- product of divergent selection pressures and/or genetic drift. In peripatric speciation (Mayr, 1954) (also commonly known as founder speciation) a small peripheral portion of the population becomes isolated and may undergo one or several (Carson, 1975) bottlenecks. Genetic drift caused by low population size during the bottlenecks together with relaxed selection pressure under the following flush phase, when the population rapidly increases in size, allows the formation of new gene combinations that would not have survived in the original population. Reproductive isolation is then believed to evolve either as a by-product of the genetic changes (Mayr, 1954; Carson, 1975; Templeton, 1980) or as a consequence of relaxation of mating preferences in bottlenecks (Kaneshiro, 1989). A more disputable model, although, recently more widely accepted (Via, 2001), is sympatric or parapatric speciation, that is, speciation without geographic isolation. Several hypotheses called “divergence-with-gene- flow speciation” (see Rice & Hostert, 1993) assume that populations become genetically isolated because traits for positive assortative mating coevolve with other traits under disruptive selection. Either selection against interbreeding is thought to build non-random associations between the genes responsible for the traits (linkage disequilibrium), or the traits represents different phenotypes deriving from the same gene (pleiotropy). The theory of “reinforcement” (Dobzhansky, 1940) implies that a feedback process between selection against hybrids and positive assortative mating reinforces reproductive isolation until the interbreeding populations have become genetically isolated. More theories of speciation are reviewed in