Publications (15)75.87 Total impact
-
Article: Exploring local immunological adaptation of two stickleback ecotypes by experimental infection and transcriptome-wide digital gene expression analysis.
[show abstract] [hide abstract]
ABSTRACT: Understanding the extent of local adaptation in natural populations and the mechanisms that allow individuals to adapt to their native environment is a major avenue in molecular ecology research. Evidence for the frequent occurrence of diverging ecotypes in species that inhabit multiple ecological habitats is accumulating, but experimental approaches to understanding the biological pathways as well as the underlying genetic mechanisms are still rare. Parasites are invoked as one of the major selective forces driving evolution and are themselves dependent on the ecological conditions in a given habitat. Immunological adaptation to local parasite communities is therefore expected to be a key component of local adaptation in natural populations. Here, we use next-generation sequencing technology to compare the transcriptome-wide response of experimentally infected three-spined sticklebacks from a lake and a river population, which are known to evolve under selection by distinct parasite communities. By comparing overall gene expression levels as well as the activation of functional pathways in response to parasite exposure, we identified potential differences between the two stickleback populations at several levels. Our results suggest locally adapted patterns of gene regulation in response to parasite exposure, which may reflect different local optima in the trade-off between the benefits and the disadvantages of mounting an immune response because of quantitative differences of the local parasite communities.Molecular Ecology 09/2012; · 5.52 Impact Factor -
Article: Genome-wide patterns of standing genetic variation in a marine population of three-spined sticklebacks.
[show abstract] [hide abstract]
ABSTRACT: Since the end of the Pleistocene, the three-spined stickleback (Gasterosteus aculeatus) has repeatedly colonized and adapted to various freshwater habitats probably originating from ancestral marine populations. Standing genetic variation and the underlying genomic architecture both have been speculated to contribute to recent adaptive radiations of sticklebacks. Here, we expand on the current genomic resources of this fish by providing extensive genome-wide variation data from six individuals from a marine (North Sea) stickleback population. Using next-generation sequencing and a combination of paired-end and mate-pair libraries, we detected a wide size range of genetic variation. Among the six individuals, we found more than 7% of the genome is polymorphic, consisting of 2 599 111 SNPs, 233 464 indels and structural variation (SV) (>50 bp) such as 1054 copy-number variable regions (deletions and duplications) and 48 inversions. Many of these polymorphisms affect gene and coding sequences. Based on SNP diversity, we determined outlier regions concordant with signatures expected under adaptive evolution. As some of these outliers overlap with pronounced regions of copy-number variation, we propose the consideration of such SV when analysing SNP data from re-sequencing approaches. We further discuss the value of this resource on genome-wide variation for further investigation upon the relative contribution of standing variation on the parallel evolution of sticklebacks and the importance of the genomic architecture in adaptive radiation.Molecular Ecology 07/2012; · 5.52 Impact Factor -
Article: Divergent selection on locally adapted major histocompatibility complex immune genes experimentally proven in the field.
[show abstract] [hide abstract]
ABSTRACT: Although crucial for the understanding of adaptive evolution, genetically resolved examples of local adaptation are rare. To maximize survival and reproduction in their local environment, hosts should resist their local parasites and pathogens. The major histocompatibility complex (MHC) with its key function in parasite resistance represents an ideal candidate to investigate parasite-mediated local adaptation. Using replicated field mesocosms, stocked with second-generation lab-bred three-spined stickleback hybrids of a lake and a river population, we show local adaptation of MHC genotypes to population-specific parasites, independently of the genetic background. Increased allele divergence of lake MHC genotypes allows lake fish to fight the broad range of lake parasites, whereas more specific river genotypes confer selective advantages against the less diverse river parasites. Hybrids with local MHC genotype gained more body weight and thus higher fitness than those with foreign MHC in either habitat, suggesting the evolutionary significance of locally adapted MHC genotypes.Ecology Letters 05/2012; 15(7):723-31. · 17.56 Impact Factor -
Article: New(t)s and views from hybridizing MHC genes: introgression rather than trans-species polymorphism may shape allelic repertoires.
[show abstract] [hide abstract]
ABSTRACT: One of the key features of major histocompatibility complex (MHC) genes is the frequent occurrence of trans-species polymorphism, that is 'the passage of allelic lineages from ancestral to descendant species' (Klein et al. 2007). Selectively maintained ancestral polymorphism may, however, be hard to distinguish from introgression of MHC alleles between hybridizing species (Fig. 1). In this issue of Molecular Ecology, Nadachowska-Brzyska et al. (2012) present data that suggest that the latter can be observed in two closely related species of newts, Lissotriton vulgaris (Lv) and L. montandoni (Lm) from south-east Europe. Strikingly, allelic MHC variation displayed more structure between geographically separated populations of L. vulgaris than across species in the hybrid zone. This suggests that high MHC variation in L. montadoni may result from mainly unidirectional gene flow between species, while differentiation between northern and southern populations of L. vulgaris might reflect local adaptation.Molecular Ecology 02/2012; 21(4):779-81. · 5.52 Impact Factor -
Article: Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations
[show abstract] [hide abstract]
ABSTRACT: The genes of the major histocompatibility complex are the most polymorphic genes in vertebrates, with more than 1,000 alleles described in human populations. How this polymorphism is maintained, however, remains an evolutionary puzzle. Major histocompatibility complex genes have a crucial function in the adaptive immune system by presenting parasite-derived antigens to T lymphocytes. Because of this function, varying parasite-mediated selection has been proposed as a major evolutionary force for maintaining major histocompatibility complex polymorphism. A necessary prerequisite of such a balancing selection process is rapid major histocompatibility complex allele frequency shifts resulting from emerging selection by a specific parasite. Here we show in six experimental populations of sticklebacks, each exposed to one of two different parasites, that only those major histocompatibility complex alleles providing resistance to the respective specific parasite increased in frequency in the next host generation. This result demonstrates experimentally that varying parasite selection causes rapid adaptive evolutionary changes, thus facilitating the maintenance of major histocompatibility complex polymorphism.Nature Communications. 01/2012; 3:621. -
Article: Induction of diploid gynogenesis in an evolutionary model organism, the three-spined stickleback (Gasterosteus aculeatus).
[show abstract] [hide abstract]
ABSTRACT: Rapid advances in genomics have provided nearly complete genome sequences for many different species. However, no matter how the sequencing technology has improved, natural genetic polymorphism complicates the production of high quality reference genomes. To address this problem, researchers have tried using artificial modes of genome manipulation such as gynogenesis for fast production of inbred lines. Here, we present the first successful induction of diploid gynogenesis in an evolutionary model system, the three-spined sticklebacks (Gasterosteus aculeatus), using a combination of UV-irradiation of the sperm and heat shock (HS) of the resulting embryo to inhibit the second meiotic division. Optimal UV irradiation of the sperm was established by exposing stickleback sperm to a UV- light source at various times. Heat shock parameters like temperature, duration, and time of initiation were tested by subjecting eggs fertilized with UV inactivated sperm 5, 10, 15, 20, 25, or 30 minutes post fertilization (mpf) to 30°C, 34°C, or 38°C for 2, 4, 6 or 8 minutes. Gynogen yield was highest when stickleback eggs were activated with 2 minutes UV-irradiated sperm and received HS 5 mpf at 34°C for 4 minutes. Diploid gynogenesis has been successfully performed in three-spined stickleback. This has been confirmed by microsatellite DNA analysis which revealed exclusively maternal inheritance in all gynogenetic fry tested. Ploidy verification by flow cytometry showed that gynogenetic embryos/larvae exhibiting abnormalities were haploids and those that developed normally were diploids, i.e., double haploids that can be raised until adult size.BMC Developmental Biology 09/2011; 11:55. · 2.79 Impact Factor -
Article: Female choice for heterozygous mates changes along successive matings in a lizard.
[show abstract] [hide abstract]
ABSTRACT: Female mate choice and female multiple mating are major focuses of studies on sexual selection. In a multiple mating context, the benefits of mate choice can change along successive matings, and female choice would be expected to change accordingly. We investigated sequential female mate choice in the moderately polyandrous common lizard (Zootoca vivipara, synonym Lacerta vivipara). Along successive mating opportunities, we found that females were relatively unselective for the first mate, but accepted males of higher heterozygosity for subsequent mating, consistent with the trade-up choice hypothesis. We discuss the evidence of trade-up mate choice in squamates and generally trade-up for mate heterozygosity in order to motivate new studies to fill gaps on these questions.Behavioural processes 09/2011; 88(3):149-54. · 1.53 Impact Factor -
Article: Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes
[show abstract] [hide abstract]
ABSTRACT: Ecological speciation has been the subject of intense research in evolutionary biology but the genetic basis of the actual mechanism driving reproductive isolation has rarely been identified. The extreme polymorphism of the major histocompatibility complex (MHC), probably maintained by parasite-mediated selection, has been proposed as a potential driver of population divergence. We performed an integrative field and experimental study using three-spined stickleback river and lake ecotypes. We characterized their parasite load and variation at MHC class II loci. Fish from lakes and rivers harbor contrasting parasite communities and populations possess different MHC allele pools that could be the result of a combined action of genetic drift and parasite-mediated selection. We show that individual MHC class II diversity varies among populations and is lower in river ecotypes. Our results suggest the action of homogenizing selection within habitat type and diverging selection between habitat types. Finally, reproductive isolation was suggested by experimental evidence: in a flow channel design females preferred assortatively the odor of their sympatric male. This demonstrates the role of olfactory cues in maintaining reproductive isolation between diverging fish ecotypes.Evolutionary Ecology. 01/2011; 25(3):605-622. -
Article: Population-specificity of heat stress gene induction in northern and southern eelgrass Zostera marina populations under simulated global warming.
[show abstract] [hide abstract]
ABSTRACT: Summer heat waves have already resulted in mortality of coastal communities, including ecologically important seagrass meadows. Gene expression studies from controlled experiments can provide important insight as to how species/genotypes react to extreme events that will increase under global warming. In a common stress garden, we exposed three populations of eelgrass, Zostera marina, to extreme sea surface temperatures, simulating the 2003-European heat wave. Populations came from locations widely differing in their thermal regime, two northern European locations [Ebeltoft (Kattegat), Doverodde (Limfjord, Baltic Sea)], and one southern population from Gabicce Mare (Adriatic Sea), allowing to test for population specificity in the response to a realistic heat stress event. Eelgrass survival and growth as well as the expression of 12 stress associated candidate genes were assessed during and after the heat wave. Contrary to expectations, all populations suffered equally from 3 weeks of heat stress in terms of shoot loss. In contrast, populations markedly differed in multivariate measures of gene expression. While the gene expression profiles converged to pre-stress values directly after the heat wave, stress correlated genes were upregulated again 4 weeks later, in line with the observed delay in shoot loss. Target genes had to be selected based on functional knowledge in terrestrial plants, nevertheless, 10/12 genes were induced relative to the control treatment at least once during the heat wave in the fully marine plant Z. marina. This study underlines the importance of realistic stress and recovery scenarios in studying the impact of predicted climate change.Molecular Ecology 07/2010; 19(14):2870-83. · 5.52 Impact Factor -
Article: RSCA genotyping of MHC for high-throughput evolutionary studies in the model organism three-spined stickleback Gasterosteus aculeatus.
[show abstract] [hide abstract]
ABSTRACT: In all jawed vertebrates, highly polymorphic genes of the major histocompatibility complex (MHC) encode antigen presenting molecules that play a key role in the adaptive immune response. Their polymorphism is composed of multiple copies of recently duplicated genes, each possessing many alleles within populations, as well as high nucleotide divergence between alleles of the same species. Experimental evidence is accumulating that MHC polymorphism is a result of balancing selection by parasites and pathogens. In order to describe MHC diversity and analyse the underlying mechanisms that maintain it, a reliable genotyping technique is required that is suitable for such highly variable genes. We present a genotyping protocol that uses Reference Strand-mediated Conformation Analysis (RSCA), optimised for recently duplicated MHC class IIB genes that are typical for many fish and bird species, including the three-spined stickleback, Gasterosteus aculeatus. In addition we use a comprehensive plasmid library of MHC class IIB alleles to determine the nucleotide sequence of alleles represented by RSCA allele peaks. Verification of the RSCA typing by cloning and sequencing demonstrates high congruency between both methods and provides new insight into the polymorphism of classical stickleback MHC genes. Analysis of the plasmid library additionally reveals the high resolution and reproducibility of the RSCA technique. This new RSCA genotyping protocol offers a fast, but sensitive and reliable way to determine the MHC allele repertoire of three-spined sticklebacks. It therefore provides a valuable tool to employ this highly polymorphic and adaptive marker in future high-throughput studies of host-parasite co-evolution and ecological speciation in this emerging model organism.BMC Evolutionary Biology 02/2009; 9:57. · 3.52 Impact Factor -
Article: Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes.
[show abstract] [hide abstract]
ABSTRACT: Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best-adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes--'magic traits'. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC-based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC-based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super-optimal individual MHC diversity and should therefore suffer more from parasites in all habitats.Ecology Letters 02/2009; 12(1):5-12. · 17.56 Impact Factor -
Article: RSCA genotyping of MHC for high-throughput evolutionary studies in the model organism three-spined stickleback Gasterosteus aculeatus
[show abstract] [hide abstract]
ABSTRACT: Abstract Background In all jawed vertebrates, highly polymorphic genes of the major histocompatibility complex (MHC) encode antigen presenting molecules that play a key role in the adaptive immune response. Their polymorphism is composed of multiple copies of recently duplicated genes, each possessing many alleles within populations, as well as high nucleotide divergence between alleles of the same species. Experimental evidence is accumulating that MHC polymorphism is a result of balancing selection by parasites and pathogens. In order to describe MHC diversity and analyse the underlying mechanisms that maintain it, a reliable genotyping technique is required that is suitable for such highly variable genes. Results We present a genotyping protocol that uses Reference Strand-mediated Conformation Analysis (RSCA), optimised for recently duplicated MHC class IIB genes that are typical for many fish and bird species, including the three-spined stickleback, Gasterosteus aculeatus . In addition we use a comprehensive plasmid library of MHC class IIB alleles to determine the nucleotide sequence of alleles represented by RSCA allele peaks. Verification of the RSCA typing by cloning and sequencing demonstrates high congruency between both methods and provides new insight into the polymorphism of classical stickleback MHC genes. Analysis of the plasmid library additionally reveals the high resolution and reproducibility of the RSCA technique. Conclusion This new RSCA genotyping protocol offers a fast, but sensitive and reliable way to determine the MHC allele repertoire of three-spined sticklebacks. It therefore provides a valuable tool to employ this highly polymorphic and adaptive marker in future high-throughput studies of host-parasite co-evolution and ecological speciation in this emerging model organism.BMC Evolutionary Biology. 01/2009; -
Article: Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity.
[show abstract] [hide abstract]
ABSTRACT: Individual diversity at the major histocompatibility complex (MHC) is predicted to be optimal at intermediate rather than at maximal levels. We showed previously in sticklebacks that an intermediate MHC diversity is predominant in natural populations and provides maximal resistance in experimental multiple parasite infections in the laboratory. However, what counts ultimately is the lifetime reproductive success (LRS). Here, we measured LRS of six laboratory-bred sib-groups-to minimize the influence of non-MHC genes-three-spined sticklebacks (Gasterosteus aculeatus) during their entire breeding period, each in a seminatural enclosure in the lake of their parents, where they were exposed to the natural spectrum of parasites. We collected developing clutches at regular intervals and determined parenthood for a representative number of eggs (2279 in total) per clutch with 18 microsatellites. Both males and females with an intermediate MHC class IIB variant number had the highest LRS. The mechanistic link of MHC diversity and LRS differed between the sexes: in females, we found evidence for a trade-off between number of eggs and immunocompentence, whereas in males this correlation was concealed by different timing strategies of reproduction.Proceedings of the Royal Society B: Biological Sciences 12/2008; 276(1658):925-34. · 5.41 Impact Factor -
Article: Condition dependence of reproductive strategy and the benefits of polyandry in a viviparous lizard.
[show abstract] [hide abstract]
ABSTRACT: Species in which males do not contribute to reproduction beyond the provision of sperm offer good opportunities to study the potential genetic benefits that females can obtain from polyandry. Here, we report the results of a study examining the relationships between polyandry and components of female fitness in the common lizard (Lacerta vivipara). We found that polyandrous females produce larger clutches than monandrous females. Polyandrous females also lose fewer offspring during the later stages of gestation and at birth, but we did not find any relationship between polyandry and physical characteristics of viable neonates. Our results were consistent with the predictions of the intrinsic male quality hypothesis, while inbreeding avoidance and genetic incompatibility avoidance might also explain some part of the variation observed in clutch size. Moreover, the benefits of polyandry appeared to depend on female characteristics, as revealed by an interaction between reproductive strategy and female length on reproductive success. Thus, all females did not benefit equally from mating with multiple males, which could explain why polyandry and monandry coexist.Proceedings of the Royal Society B: Biological Sciences 03/2007; 274(1608):425-30. · 5.41 Impact Factor -
Article: MHC-based mate choice combines good genes and maintenance of MHC polymorphism
[show abstract] [hide abstract]
ABSTRACT: Polymorphic genes of the major histocompatibility complex (MHC) are regarded as essential genes for individual fitness under conditions of natural and sexual selection. To test this hypothesis, we investigated the ultimate individual fitness trait — that of reproductive success. We used three-spined sticklebacks (Gasterosteus aculeatus) in seminatural enclosures, located in natural breeding areas where the experimental fish had been caught. During their reproductive period, fish were exposed continuously to their natural sympatric parasites. By genotyping almost 4000 eggs with nine microsatellites, we determined parenthood and inferred female mating decision. We found that with reference to their own MHC profile, female sticklebacks preferred to mate with males sharing an intermediate MHC diversity. In addition, males with a specific MHC haplotype were bigger and better at fighting a common parasite (Gyrodactylus sp.). This translated directly into Darwinian fitness since fish harbouring this specific MHC haplotype were more likely to be chosen and had a higher reproductive output. We conclude that females also based their mating decision on a specific MHC haplotype conferring resistance against a common parasite. This identifies and supports 'good genes'. We argue that such an interaction between host and parasite driving assortative mating is not only a prerequisite for negative frequency-dependent selection — a potential mechanism to explain the maintenance of MHC polymorphism, but also potentially speciation.Molecular Ecology, v.18, 3316-3329 (2009).
Top co-authors
Top Journals
Institutions
-
2012
-
Helmholtz Centre for Ocean Research Kiel
Kiel, Schleswig-Holstein, Germany -
Leibniz-Institut für Meereswissenschaften an der Universität Kiel
Kiel, Schleswig-Holstein, Germany
-
-
2008–2011
-
Max-Planck-Institut für Evolutionsbiologie
- Department of Evolutionary Ecology
Plön, Schleswig-Holstein, Germany
-
