Genetic variation in parasitoid resistance in natural populations of Drosophila melanogaster Gerritsma, Sylvia
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Genetic variation in parasitoid resistance in natural Genetic variation in parasitoid resistance in natural Genetic variation in parasitoid resistance in natural Genetic variation in parasitoid resistance in natural
populations of populations of populations of
populations of Drosophila melanogaster Drosophila melanogaster Drosophila melanogaster Drosophila melanogaster
Sylvia Gerritsma
Cover design: Sylvia Gerritsma and Fokje Nagelhout Lay-out: Sylvia Gerritsma and Iris van Halderen Printed by: Gildeprint - Enschede
ISBN (printed): 978-90-367-8310-1 ISBN (digital): 978-90-367-8309-5
The research in this thesis was carried out in the Evolutionary Genetics group at the Centre for Ecology and Evolutionary Studies (CEES) -from 2015 onwards known as The Groningen Institute for Evolutionary Life Sciences (GELIFES)- of the University of Groningen, the Netherlands, according to the requirements of the Graduate School of Science (Faculty of Mathematics and Natural Sciences, University of Groningen).
This work was supported by VIDI grant no. 864.08.008 of the Netherlands Organization for Scientific Research (NWO) to Bregje Wertheim. The printing of this thesis was partly funded by the University of Groningen and the Faculty of Mathematics and Natural Sciences.
resistance in natural populations of Genetic variation in parasitoid resistance in natural populations of
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
en
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de
en volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
geboren op 4 februari 1984
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Sylvia Gerritsma geboren op 4 februari 1984
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
Proefschrift
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
op gezag van de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Sylvia Gerritsma geboren op 4 februari 1984
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
Proefschrift
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
op gezag van de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Sylvia Gerritsma geboren op 4 februari 1984
te Vlieland
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
Proefschrift
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
op gezag van de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
door
Sylvia Gerritsma geboren op 4 februari 1984
te Vlieland
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
Proefschrift
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
op gezag van de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
door
Sylvia Gerritsma
geboren op 4 februari 1984 te Vlieland
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
Proefschrift
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
op gezag van de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Sylvia Gerritsma geboren op 4 februari 1984
te Vlieland
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
Proefschrift
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
op gezag van de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Sylvia Gerritsma geboren op 4 februari 1984
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Sylvia Gerritsma geboren op 4 februari 1984
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
geboren op 4 februari 1984
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de
rector magnificus prof. dr. E. Sterken volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op vrijdag 13 november 2015 om 11.00 uur
Genetic variation in parasitoid resistance in natural populations of
Drosophila melanogaster
ter verkrijging van de graad van doctor aan de
volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op
Genetic variation in parasitoid resistance in natural populations of
volgens besluit van het College voor Promoties.
Genetic variation in parasitoid
resistance in natural populations of
resistance in natural populations of
resistance in natural populations of
Copromotor
Dr. L.P.W.G.M. Jacobus Mgn Van De Zande
Beoordelingscommissie Prof. dr. L.W. Beukeboom Prof. dr. F. Vavre
Prof. dr. E. Decaestecker
Chapter 1 General introduction 7
Chapter 2 Natural variation in differentiated hemocytes is related to parasitoid resistance in Drosophila melanogaster
29
Chapter 3 Genetic variation in putative loci for parasitoid resistance in natural populations of Drosophila melanogaster
51
Chapter 4 Genetic variation of the immune receptor Tep1 among natural populations of Drosophila melanogaster
79
Box 1 Is the gene Tep1 involved in the encapsulation of parasitoid eggs - A functional analysis using GAL4/UAS RNAi
95
Chapter 5 Bacterial communities differ among Drosophila melanogaster populations and affect host resistance against parasitoids
105
Chapter 6 General discussion 129
Bibliography 143
Summary 165
Samenvatting 173
Acknowledgements 181
7
General introduction General introduction General introduction General introduction
Evolutionary adaptation is the process by which members of a population become better suited for particular features in their environment through heritable changes in characteristics that enhance their survival or reproduction (i.e. their fitness). Abilities such as avoidance of predators, defense against parasites and the ability to handle extreme weather conditions are coping mechanisms that have a selective advantage for organisms (i.e. fitness advantage). When coping with opposing organisms, such as predators, pathogens and other natural enemies, these opposing organisms are also constantly evolving. This can lead to a dynamic co-evolution, where reciprocal evolutionary changes occur in the different populations of the opposing organisms (the Red-Queen hypothesis, Van Halen, 1973).
Among the greatest selective forces a population of organisms experiences is that of host-parasite interactions. This is due to the strong antagonistic fitness effects of the relationship. Parasites have evolved some extraordinary adaptations for infecting hosts.
Hosts can suffer great costs from these infections by means of loss of fertility, increased morbidity and mortality, and have evolved some equally impressive adaptations to avoid or overcome infection. The parasites suffer from these host defense mechanisms in terms of development, propagation and survival. Since both antagonists impose strong selection pressures on each other, these host-parasite models can end up in either cycles of genetic change, or a runaway system of an escalation of a co-evolutionary arms race if the costs of adaptations do not outweigh the benefits (Schmid-Hempel, 2005).
In this thesis, I study the evolution of an adaptive trait in natural host populations to parasitoid attack, using Drosophila melanogaster-Asobara tabida as a host-parasitoid system. Natural populations of D. melanogaster differ strongly in their ability to resist parasitoid attack, due to local differences in the selection pressures that have been shaping the host populations. The defense mechanism that provides resistance against parasitoids consists of an immune response named melanotic encapsulation (Lavine & Strand, 2002).
My aim was to uncover the genetic basis for the natural variation in the immunological defense against parasitoids. To study this defense mechanism among natural populations of D. melanogaster and to investigate the variation of the immune response, I first collected flies from natural populations throughout Europe. Through a combination of
8
immunological assays, parasitization assays, population genetics and gene expression experiments, I investigated the underlying genetic variation of the immune response in natural populations of D. melanogaster against parasitoids. Apart from the role of genetic variation in the ability to resist parasitoid attack, the effect of the microbiome of D.
melanogaster on parasitoid resistance was also considered, by characterizing the composition and diversity of bacterial communities in the field lines.
1.1 1.1
1.1 1.1 Population genetics Population genetics Population genetics Population genetics
To uncover the genetic basis for the variation in parasitoid resistance, I compared natural populations that evolved towards different levels of parasitoid resistance. To study the genetic variation that underlies this phenotypic variation requires a population genetics approach. The field of population genetics came into existence in the early 1900s. It is the statistical application of Mendel’s laws at the level of populations of organisms. By comparing allele frequencies within and among populations, it evaluates the evolutionary processes that affected these populations. These comparisons can be used, for example, to test for evolutionary relationships between populations, how populations adapted to their environment or how non-adaptive processes have shaped the genetic composition of the populations. The evolution of populations is governed by several processes, which will be briefly described in this section. I will start with a brief description of the concepts of evolutionary processes, and how the combined processes can lead to evolutionary adaptations. Finally, I will provide a brief description of the methods that I used in my population comparisons to distinguish between adaptive and non-adaptive evolutionary processes.
1.1.1 1.1.1 1.1.1
1.1.1 Evolutionary processes affecting populations Evolutionary processes affecting populations Evolutionary processes affecting populations Evolutionary processes affecting populations
Genetic variation is the raw material for evolution to act on. The source of genetic variation is mutationmutationmutationmutation. Hartl & Clark (2007) define mutation as “the heritable change in genetic material which can be a change in nucleotide sequence as well as the formation of a chromosome rearrangement” (e.g. inversions, translocation). Mutations include the full spectrum from single base pair changes through alterations that effect longer DNA sequences, including base pair transitions, insertions and deletions, duplications, recombination, and chromosomal alternations. By means of mutations, new alleles are created which contribute to genetic variation within the population. Not all mutations are beneficial for the individual; most are in fact neutral or deleterious. Deleterious mutations have a negative effect on the organism’s fitness when expressed. Beneficial mutations have
9 a positive effect on the organism’s fitness by enhancing its survival and reproduction.
However, expression of beneficial or deleterious alleles can be conditional on specific environmental conditions. When these conditions are not met, such alleles are effectively neutral and they can accumulate in the population if not lost from the population by random genetic drift.
Random genetic driftgenetic driftgenetic drift occurs when alleles increase or decrease in frequency by genetic drift chance (Hartl & Clark, 2007). The chance that an allele fixates due to genetic drift depends on their initial frequency in the population, which in turn is related to the effective population size (i.e. the number of individuals participating in reproduction (Hartl & Clark, 2007). When the initial frequency of a mutation is low, they are likely to be removed from the population, due to random genetic drift. This process can affect beneficial and deleterious alleles, since they both usually start at a very low frequency in the population.
Random genetic drift can therefore play a significant role in evolution, whether selection plays a role or not.
Selection Selection Selection
Selection is the process where particular alleles become more (or less) abundant in the population, due to their positive (or negative) effects on reproduction or survival of the individuals, carrying those alleles. Alleles that are deleterious are removed from the population, since individuals that carry them do not or hardly contribute to the next generation. This can be referred to as negative or purifying selection. Beneficial alleles will gradually increase in frequency from generation to generation through natural selection, unless they are lost by random genetic drift. They may eventually become fixed in the population (Schlötterer, 2003). This is what is generally called positive or directional selection. Alternatively, there may be selection to maintain several alleles in the population, thus maintaining the genetic variation in the population. These processes are collectively called balancing selection (Hartl & Clark, 2007). This includes, for example, frequency dependent selection, in which mutations are only beneficial when they occur in low or high frequency, or heterozygote advantage, where individuals carrying heterozygote alleles have a fitness advantage.
Migration Migration Migration
Migration is the movement of individuals or genetic material (e.g. pollen) from one population to another. It contributes to an increase of genetic variation within a population, since new alleles are introduced through gene flow when migrants are included into the effective population. The effect of migration on a population depends on many parameters like migration rate and the number of subpopulations (Schlötterer, 2003).
While migration may increase genetic variation, it may decrease the scope for local adaptation by reducing the differentiation among populations.
In population genetics, changes in allele frequencies are estimated. The difficulty lies in distinguishing whether changes in allele frequencies are due to processes like
