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Genetic Disequilibria and the Interpretation of Population Genetic Structure in Daphnia

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Genetic Disequilibria and the Interpretation of Population Genetic Structure in Daphnia Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 668 _____________________________ _____________________________ Genetic Disequilibria and the Interpretation of Population Genetic Structure in Daphnia BY LARS M. BERG ACTA UNIVERSITATIS UPSALIENSIS UPPSALA 2001 Dissertation for the Degree of Doctor of Philosophy in Conservation Biology presented at Uppsala University in 2001. ABSTRACT Berg, L. M. 2001. Genetic disequilibria and the interpretation of population genetic structure in Daphnia. Acta Universitatis Upsaliensis. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 668. 36 pp. Uppsala. ISBN 91-554-5152-7. Understanding the processes that shape the spatial distribution of genetic variation within species is cent- ral to the evolutionary study of diversification and demography. Neutral genetic variation reflects past demographic events as well as current demographic characteristics of populations, and the correct inter- pretation of genetic data requires that the relative impact of these forces can be identified. Details of breeding systems can affect the genetic structure through effects on effective migration rate or on effect- ive population size. Restrictions in recombination rate lead to associations between neutral marker genes and genes under natural selection. Although the effects on genetic structure can be substantial, the pro- cess will often be difficult to tell apart from stochastic effects of history or genetic drift, which may sug- gest erroneous conclusions about demography. In cyclically parthenogenetic freshwater invertebrates, which alternate between sexual and asexual reproduction, demographic fluctuations and reliance on diapausing eggs for dispersal enhances neutral genetic differentiation as well as effects of selection on associated genes. Although genetic founder effects are expected to be profound and long-lasting in these species, genetic hitch-hiking may reduce initial strong differentiation rapidly if better adapted genes are introduced by mutation or immigration. Fluctuating environmental conditions have been suggested to generate rapid shifts in the frequencies of clones during the asexual phase. In the presence of egg banks resting in sediments, genetic diversity is stabilised and the importance of migration for differentiation is reduced. Studies of unstable and young populations of cyclically parthenogenetic Daphnia pulex showed substantial variation for important fitness traits, within as well as between populations, despite hypothes- ised recent founder effects. Neutral markers indicated genetic equilibrium, but changes in clonal compo- sition during asexuality disrupted the genetic structure in a manner compatible with local adaptation and exclusion of immigrants. This illustrates that the forces affecting sexual progeny may be markedly differ- ent from those shaping the structure among asexual individuals. Key words: Breeding system, linkage disequilibrium, dispersal, genetic structure, Daphnia pulex Lars Berg, Department of Conservation Biology and Genetics, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden © Lars Berg 2001 ISSN 1104-232X ISBN 91-554-5152-7 Printed in Sweden by Uppsala University, Tryck & Medier, Uppsala 2001 Preface This thesis is based on the following papers, which will be referred to in the text by their Roman numerals: I Berg LM & Lascoux M (2000) Neutral genetic differentiation in an island model with cyclical parthenogenesis. Journal of Evolutionary Biology 13: 488-494. II Berg LM (submitted) Selection and differentiation in cyclically parthenogenetic species. I. Hitch-hiking with sweeping allele. III Berg LM (submitted) Selection and differentiation in cyclically parthenogenetic species. II. Fluctuating selection and egg banks. IV Berg LM, Pálsson S & Lascoux M (2001) Fitness and sexual response to population density in Daphnia pulex. Freshwater Biology 46: 667-677. V Berg LM, Lascoux M & Bengtsson J (submitted) Local genetic structure for microsatellites as indicator of demographic and selective processes in Daphnia pulex. Reprints were made with permission from Blackwell Scientific Publishers © Contents Sammanfattning Teori......................................................................................................................1 Empiri....................................................................................................................3 Slutsatser...............................................................................................................4 Introduction The origin of genetic structure................................................................................7 Measuring genetic structure....................................................................................8 Interpreting genetic structure..................................................................................9 Daphnia as a model organism...............................................................................12 Aims and outline of the thesis................................................................................13 Theoretical studies Neutral differentiation with cyclical parthenogenesis (I)......................................14 Selection and differentiation in Daphnia (II, III)..................................................16 Empirical studies Geographic structure for fitness traits in Daphnia pulex (IV)..............................22 Geographic structure for neutral genes in Daphnia pulex (V)..............................25 Conclusions....................................................................................................................29 References.......................................................................................................................30 Acknowledgements.........................................................................................................36 “Problems in science are sometimes made easier by adding complications” Daniel C Dennett Dedicated with love to Gösta Sædén (1917-1994), my first and best example of the scientific mind Sammanfattning Ekologiska tolkningar av populationsgenetiken hos hinnkräftor DET ÄR en allmän uppfattning att Charles området molekylärekologi, som studerar Darwins idé om det naturliga urvalet revolu- sambanden mellan genetik och bl a demo- tionerade biologin. Detta stämmer förvisso, grafi. men är bara halva sanningen. Kanske ännu viktigare var hans insikt om betydelsen av den naturliga variation som finns mellan in- Teori divider inom arter, för utan variation kan För att gå från genetik till demografi krävs inget urval ske. Medan biologer före Darwin modeller som på ett förenklat sätt beskriver brukade se de avvikande exemplaren som hur förhållandet dem emellan borde se ut i anomalier och brott mot naturens ordning, olika situationer. Problemet med enkla vet- ser man numera variationen som en förut- enskapliga modeller är dock att det kan vara sättning för livets utveckling. Uppkomsten svårt att bedöma deras tillförlitlighet, efter- av nya arter förklaras allmänt med att växt- som även dåliga modeller kan ge resultat och djurbestånd delas upp i mindre grupper, som ser ut att vara vettiga, fastän de är varpå urvalet och slumpeffekter får dessa att missvisande. Inom populationsgenetiken är bli mer och mer olika varandra. I processen det t ex vanligt att man utgår från att olika omvandlas genetiskt betingad variation inom krafter är i jämvikt med varandra, så att man grupper till variation mellan grupper och – i kan bortse från svårkontrollerade historiska förlängningen – mellan arter. skeden. Samtidigt blir ekvationerna ofta lätt- Att förstå de processer som bestämmer are att lösa. fördelningen av genetisk variation i tid och När man så beskriver hur utbyte av rum är alltså grundläggande för evolutions- individer mellan populationer påverkar deras biologin. Här bidrar populationsgenetiska populationsgenetiska struktur, är det vanligt studier med en väsentlig del, nämligen med att man tillgriper modeller som bygger på en förståelsen av de fenomen som styr varia- jämvikt mellan de krafter som gör popula- tionen hos specifika gener inom popula- tionerna genetiskt olika och de som håller tioner. Man studerar ofta noggrant utvalda ihop dem. Det är framför allt förändringar i gener som fungerar som “markörer” för olika arvsanlagen, d v s mutationer, och slump- egenskaper. De flesta markörer kan även an- mässig förlust av varianter – så kallad gene- vändas till att indikera släktskap mellan tisk drift – som leder till genetisk olikhet, individer, vilket är en av populationsgene- medan likhet främjas av spridning mellan tikens viktigaste tillämpningar. Teorin kring populationer. Vidare kan naturligt urval släktskapsmarkörer handlar i grunden om verka åtskiljande eller sammanhållande, be- enkel folkräkning, eller demografi med ett roende på hur miljöfaktorerna varierar annat ord. Det kan gälla att t ex ta reda på mellan populationerna. Populationer kan hur många individer det finns, hur bra de är alltså vara lika varandra antingen för att de på att föröka sig och hur de rör sig i land- regelbundet utbyter individer, eller för att de skapet, kunskaper som bl a är eftertraktade utbytt individer tills helt nyligen, där inom naturvårdsarbetet. Dessutom hjälper “nyligen” i princip kan betyda allt från förra sådana insikter ekologer att bättre förstå de fältsäsongen till tiden för senaste inlandsisen, processer som ligger bakom arters utbred- beroende
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