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University of Groningen Spatial Arrangement of Genetic Variation In University of Groningen Spatial arrangement of genetic variation in the marine bivalve Macoma balthica (L.) Luttikhuizen, Pieternella Christina IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2003 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Luttikhuizen, P. C. (2003). Spatial arrangement of genetic variation in the marine bivalve Macoma balthica (L.). s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 04-10-2021 Garamond,Bold Garamond,Italic Garamond Garamond,BoldItalic Garamond Identity-H: цθ SpatialGaramond arrangement MacRoman: of åº πgeneticσ2ΦΦ°⊂χµ ·variation≤∞δ in the marineTimesNewRoman bivalve Identity-H Macoma: цθbalthica (L.) Times New Roman TimesNewRoman-Italics Arial Arial Arial Arial Symbol Identity-H: Σψµβολ Ιδεντιτψ−Η: θ Courier −bx −bx 2 ay(1 − e ) bx + ay(1 − e ) ∂ P ebx − aye + (ay −1)e ⇒ = −ab()s ∂ ∂ ∑ − −bx x y 2bx − + ay(1 e ) 2 e ( 1 e ) Pieternella C. Luttikhuizen Spatial arrangement of genetic variation in the marine bivalve Macoma balthica (L.) Figures: with help from D. Visser and J. Drent Printed by: Drukkerij van Denderen BV, Groningen ISBN: 90-367-1742-6 The work presented in this thesis was carried out at the Royal Netherlands Institute for Sea Research, Department of Marine Ecology, and the University of Groningen, Centre for Ecological and Evolutionary Studies. RIJKSUNIVERSITEIT GRONINGEN ‘Spatial arrangement of genetic variation in the marine bivalve Macoma balthica (L.)’ Proefschrift ter verkrijging van het doctoraat in de Wiskunde en Natuurwetenschappen aan de Rijksuniversiteit Groningen op gezag van de Rector Magnificus, dr F. Zwarts, in het openbaar te verdedigen op vrijdag 17 januari 2003 om 16:00 uur door Pieternella Christina Luttikhuizen geboren op 22 april 1972 te Middelburg Promotor: Prof. Dr W. van Delden Co-promotor: Dr T. Piersma Beoordelingscommissie: Prof. Dr J.L. Olsen Prof. Dr A.J. Baker Prof. Dr R.F. Hoekstra ISBN: 90-367-1742-6 voor mijn moeder Christien CONTENTS PART A Spatial genetic variation 9 ONE General introduction 19 TWO Population divergences predate last glacial maximum in 21 Europe for a marine bivalve with pelagic larval dispersal P.C. Luttikhuizen, J. Drent and A.J. Baker (submitted) THREE Spatially structured genetic variation in a broadcast spawning 43 bivalve: quantitative versus molecular traits P.C. Luttikhuizen, J. Drent, W. van Delden and T. Piersma (Journal of Evolutionary Biology, in press) Box I Differential selection due to bird predation may help 63 maintain marine biodiversity P.J. van den Hout, P.C. Luttikhuizen, Y. Afeworki and T. Piersma (manuscript) FOUR A technical solution to heterozygote deficiencies in the 67 bivalve Macoma balthica P.C. Luttikhuizen (manuscript) PART B External fertilization 81 FIVE Optimal egg size for external fertilization: theory on the role 83 of sperm limitation and field observations for a marine bivalve P.C. Luttikhuizen, P.J.C. Honkoop, J. Drent and J. van der Meer (submitted) Box II Survival and anisogamy 99 M.G. Bulmer, P.C. Luttikhuizen and G.A. Parker (Trends in Ecology and Evolution 17: 357-358) SIX Temporal and spatial variation in spawning of Macoma balthica 103 J. Drent and P.C. Luttikhuizen (manuscript) SEVEN Fertilization in broadcast spawning marine bivalves is a 117 small scale process: the Baltic clam Macoma balthica P.C. Luttikhuizen and J. Drent (manuscipt) EIGHT Mosaic haploid-diploid embryos and polyspermy in the 127 tellinid bivalve Macoma balthica P.C. Luttikhuizen and L.P. Pijnacker (Genome 45: 59-62) NINE General discussion 133 BIBLIOGRAPHY 146 SUMMARY 165 SAMENVATTING 171 AUTHOR ADDRESSES/PRESENT ADDRESS 180 PUBLICATION LIST 181 DANKWOORD 182 CHAPTER ONE General introduction Intraspecific genetic variation forms the raw material for evolution. Without heritable variation, evolution by means of natural selection would not occur. The spatial separation of genetic variation has two sides: it can maintain variation for selection, and it can also be the result of selection. This thesis addresses the question: ‘What does a life history of external fertilization and pelagic larval dispersal imply for the spatial arrangement of intraspecific genetic variation?’’ The spatial arrangement of intraspecific genetic variation is partly dependent on the amount of genetic exchange (gene flow) between different spatial units (e.g., populations). This is the case for both neutral genetic variation and genetic variation under the influence of selection. Traditionally, isolation was viewed by many authors, of whom Mayr was the main advocate (e.g. Mayr 1942, 1963), as a necessary first step in differentiation. This rather extreme conception was relaxed in later years into one of degree: how much gene flow is sufficient to prevent differentiation (e.g. Ehrlich and Raven 1969, Slatkin 1987, Lenormand 2002)? If all taxa were linearly arranged along a continuous gradient describing the amount of gene flow, marine broadcast spawning invertebrates would be placed near one extreme end of the gradient, with their high levels of genetic exchange. This makes these invertebrates useful for testing predictions of population genetic models in relation to gene flow. This thesis aims to do this, with particular emphasis on the difference between differentiation in neutral and selective variation in the face of gene flow. The bivalve Macoma balthica (L.) or Baltic clam was chosen as the model species for this, as it has been previously well studied in marine benthic ecology, with a focus on its population dynamics, community ecology, population structure and evolutionary ecology (e.g. Lammens 1967, Hulscher 1973, Beukema 1993, Hummel et al. 1995, Honkoop et al. 1998, Edelaar 2000, De Goeij et al. 2001, Van der Meer et al. 2001, Drent 2002, Hiddink and Wolff 2002). In this thesis the term ‘population’ is used throughout. This suggests there is a scale at which a species can be surveyed to reveal a discrete set of populations that have complete mixing within them and some fixed amount of exchange between them. In reality, intraspecific structure tends to be much more complex. The species studied here can be distributed continuously (e.g. across large stretches of mudflat such as those in the Wadden Sea) or discontinuously (e.g. in river estuaries on a predominantly rocky shore coastline). It is nevertheless insightful to approach population structure with an island-mainland model that assumes discrete populations. Such a model is easier to deal with mathematically than more complex models, and, in the absence of prior knowledge, it can serve well as the simplest possible alternative to a null hypothesis of the absence of population subdivision. 9 Genetic variation within and among populations Genetic variation arises due to mutation. In most species, there is abundant spatial differentiation in gene frequencies, and two of the main aims of evolutionary biology are to understand how spatial genetic differentiation originates and how it is maintained. The reverse is also true; spatial separation is one of the forces that helps to maintain genetic variation. Different forces are continually at work, some tend to produce differentiation, while others tend to produce homogenization. The amount of spatial differentation that results depends on the balance between these forces. The nature of the forces involved in local differentiation differs between so-called neutral and selective genetic variation. The distinction between neutral and selective (non-neutral) variation can be problematic due to the transition zone between them. The crucial difference between the two, as applied in the context of functional biological questions, is that in selective variation, the alternative genetic variants are directly associated with a difference in phenotype and functionality (e.g., biochemically, ecologically). For neutral variation this is not the case. While some authors rank for instance silent substitutions in protein coding DNA and codon bias under neutral variation because it bears no direct relationship to the biological functioning of the individual, others may view these examples as selective variation, e.g. when trying to explain GC content of DNA. In this thesis, silent substitutions in mitochondrial protein coding DNA as well as allozyme variants are treated as neutral genetic variation, although the assumed neutrality of the allozymes is discussed in chapter 9. Non-neutral variation
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