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Etienne Loire
Centre National de la Recherche Scientifique
Institut des sciences de l'évolution de Montpellier
France

Evolution of two multigene families involved in subspecies recognition and sexual isolation in the house mouse: insights from a transcriptomic and genomic perspective

poster 

Author(s): Loire, E, Boursot, P, Smadja, C

Summary:

The two subspecies of the house mouse Mus musculus musculus and M. m. domesticus have evolved in allopatry for half a million years before meeting secondarily in Europe 5000 years ago, forming a narrow hybrid zone with unfit hybrids. Previous studies have shown that these incipient species recognise each other through signals present in urine and mate assortatively in the contact zone. This suggests a reinforcement process in this zone where prezygotic isolation would evolve as a response to selection against hybridisation. Our study addresses the genetic basis of sexual isolation between these two subspecies by analyzing divergence of two large multigene families involved in chemosensory recognition. On the signaling side, we focused on the Major Urinary Proteins (MUP), a cluster of more than 21 duplicated genes known to act as pheromones in the house mouse. On the reception side, we focused on their potential receptors, the vomeronasal receptors (VR), a very large multigene family composed of more than 200 genes, expressed in the vomeronasal organ of the mouse and known to be involved in pheromone recognition. Since assortative mating is displayed in the hybrid zone, we predicted strong sign of divergence between the two subspecies at our candidate families provided that they are involved in sexual isolation. Moreover, if reinforcing selection is acting on the mate recognition system in the hybrid zone, we expected a stronger signature of selection in the genomic regions baring VR and MUP genes in individuals of the hybrid zone as compared to individuals residing in allopatric zones of the distribution range. By combining several high-throughput genomic methods such as RNA-seq and exome sequencing, we tested these predictions and explored divergence affecting the VR and MUP gene families at the sequence, expression and structural levels.

Thierry Wirth
Muséum National d'Histoire Naturelle - EPHE
Department of Systematics and Evolution
France

Genetic structure, selection and duplication in European eels MHC class II genes

poster 

Author(s): Wirth, T, Galan, M, Delgado, SF, Gilabert, A

Summary:

Understanding adaptation and selection in populations facing environmental changes is a major concern. Our project aims to understand the adaptation and resilience of endangered catadromous European eel to increasing parasitic pressure. Anguilla anguilla has encountered successive waves of exotic invasive parasites, namely, the swimbladder nematode Anguillicoloides crassus. Infested individuals have high swimming performance costs; and might fail to complete the reproductive migration back to the Sargasso Sea. Prevalence of such parasites is much higher in the naive European populations compared to native Japanese hosts. However, the nature of the ongoing adaptation and impact on eel’s biology remain largely unknown. Given the role of Major Histocompatibility Complex (MHC) genes in host–parasite interactions, we designed specific primers to sequence 2 class II exons. Using NGS, we sampled alleles from 12 European populations (N = 120) collected throughout the species distribution range, as well as from one American population (N=10). Additional historical samples (1874) from Charente were included. Our results indicate success in isolating relevant MHC class II genes; we identified respectively 149 and 154 DAA and DAB MHC class II alleles. The multiple copy nature of the MHC loci was confirmed, with at least 4 and 5 gene copies for DAA and DAB loci, respectively. European and American eels were found to share the same allelic pool, a result in sharp contrast with microsatellite data, suggesting that balancing selection is acting on these genes while ancient polymorphisms is retained within the Atlantic lineages. There was no evidence for temporally fluctuating selection pressure. Finally, the eel MHC class II exons appeared to be under positive selection and at the upper range of rho and omega values in teleosts. These results suggest that recent duplications occurred in the genus that might have facilitated inter-locus recombination and high allelic diversity.

Elena Marmesat-Bertoli
Estación Biológica de Doñana-CSIC
Department of Integrative Ecology
Spain

Low genetic diversity in MHC loci in the critically endangered Iberian lynx

poster 

Author(s): Marmesat-Bertoli, E, Mazzoni, C, Soriano, L, Sommer, S, Godoy, JA

Summary:

A central premise in Conservation Genetics is that genetic erosion occurring in declining populations reduces adaptive potential and compromises viability. However, functional variation is seldom assessed in endangered populations. Here we use the Major Histocompatibility Complex class I and II-DRB loci (MHC) as functional model loci to study the impact of the decline on Iberian lynx genetic variation, a species for which previous genetic studies have shown a strong decline in the neutral variation and concomitant fitness reductions.

We genotyped the most variable exon of MHC I and II-DRB genes in 300 individuals from the two extant wild and the captive populations using a 454 platform and a new pipeline analysis. We used transcriptomic and genomic data for primer design and expression analysis. Captive individuals, having a well-established pedigree, allowed us to infer composite haplotypes and to analyse segregation. We found a total of 13 and 6 alleles probably corresponding to 7 and 3 loci for MHCI and MHCII, respectively. One allele shows signals of pseudogenization and not all other alleles were confirmed to be expressed. In the case of MHCII, most individuals in the smallest and less diverse Doñana population show a three-allele profile, consistent with homozygosity at all three loci. Additionally global diversity levels for MCH_I and II are low compared to other felid species.

Our results suggest that the immune response in remnant Iberian lynx populations may be compromised and that the severe reduction and fragmentation may have eroded not only the neutral, but also the functional genomic diversity, thus compromising the evolutionary adaptive potential of the species.

Melinda Hofmann
National Museum of Natural Sciences (MNCN)
Department of Biodiversity and Evolutionary Biology
Spain

MHC Evolution in Neotropical Cichlids (Amphilophus sp.)

poster 

Author(s): Hofmann, MJ, Bracamonte, SE, Eizaguirre, C, Barluenga, M

Summary:

The Major Histocompatibility Complex (MHC) is a key component of the adaptive immune system of all vertebrates. Considerable evidence has accumulated suggesting that parasite-mediated selection acting on MHC genes may ultimately lead to speciation. The Midas cichlid species complex of the crater lakes of Nicaragua is an ideal model system for the study of speciation, because it has recently colonized several isolated crater lakes where it has independently diverged into sympatric sister species. We evaluate the hypothesis that host parasite interactions might be contributing to the speciation process in this system. To this end we have characterized and sequenced the MHC class IIB of individuals from different putative species of this cichlid species complex.

Arnaud Gaigher
University of Lausanne
Department of Ecology and Evolution
Switzerland

MHC evolutionary ecology in European barn owls (Tyto alba)

poster 

Author(s): Gaigher, A, Burri, R, Roulin, A, Fumagalli, L

Summary:

Major histocompatibility complex (MHC) genes play an essential role in the adaptive immune response and thus constitute a good model to study adaptive genetic variability. The extraordinary diversity exhibited by MHC genes is thought to be maintained by pathogen-driven selection, for which three hypotheses have been proposed: rare-allele advantage, heterozygote advantage and fluctuating selection. Despite a growing amount of empirical data, it is still difficult to distinguish the relative role of the different forms of selection in maintaining MHC variability. Moreover other mechanisms such as sexual selection through mate choice can shape the MHC diversity. The barn owl (Tyto alba) exhibits a number of characteristics that make it an ideal model to study MHC diversity. Indeed it is one of the most widespread birds worldwide and it has been shown that this species exhibits mate choice related to an ornamental trait that is associated to parasite resistance. In addition, this bird possesses a relatively simple MHC organization, and is one of only few species in which the two functional MHC class IIB genes can be amplified specifically. Using 454 technology, we sequenced exon 2 of the two MHC class IIB loci in a large number of individuals sampled throughout Europe (N=384) and Switzerland (N=960), for the latter of which information related to individual fitness is available (e.g. immunocompetence, parasite fecundity). We examined the effects of particular alleles and MHC diversity on these fitness parameters. First results indicate a positive effect of heterozygosity on parasite resistance, in agreement with expectations of the heterozygote advantage hypothesis. With the sampling across Europe we will be able to study spatial patterns of MHC diversity and evaluate if MHC genotypes are locally adapted or under balancing selection at the spatial scale. Therefore, this study provides interesting perspectives for the understanding of MHC evolutionary ecology.

Marco Galaverni
Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA)
Italy

MHC variability and mate choice in a recovering wolf population

poster 

Author(s): Galaverni, M, Caniglia, R, Lapalombella, S, Fabbri, E, Randi, E

Summary:

Isolated small populations might experience low adaptability and increased extinction risks due to reduced genetic variability, especially if at important functional genes such as the Major Histocompatibility Complex (MHC). We investigated for the first time the variability of three class-II genes (DRB1, DQA1, DQB1) in the Italian wolf population, which was long isolated and is now expanding after a recent bottleneck. Compared to other populations, we still found a remarkable MHC variability with 6 to 9 alleles per locus, showing signatures of historical selection (high dN/dS ratio). The Italian wolves are known to hybridize with domestic dogs, and dog-derived MHC alleles were detected in some genetically-admixed individuals. Background microsatellite and MHC loci did not show reduced variability due to the recent bottleneck. Thus, the population recovery seems not to be threatened by reduced MHC variation nor by deep domestic dog allele introgression. The observed variability could be also influenced by reproductive patterns, which can rely upon MHC similarity between mates. Based on pedigree data of wild-living packs, as reconstructed from extensive non-invasive genetic sampling, we tested the hypothesis of non-random mate choice in 26 breeding pairs. Unexpectedly, the results showed a prevalence of MHC-based assortative mating, with excess of peptide similarity between breeding pair members as compared to random expectations. Moreover, variation in both relatedness and heterozygosity showed significant positive correlations with fitness traits (total offspring, years as reproducers, mean offspring per year) deduced from pedigrees. These findings suggest possible advantages for breeders that are more related at the MHC, but not at the genetic background. This balance of general inbreeding avoidance, MHC-assortative mating and heterozygote advantage can reflect the social structure of the species, potentially maximizing the adaptation to the environmental pressures

Irem Sepil
University of Oxford
Department of Zoology
United Kingdom

MHC-based qualitative and quantitative resistance to avian malaria in a wild bird population

poster 

Author(s): Sepil, I, Lachich, S, Hinks, AE, Sheldon, BC

Summary:

Major histocompatibility complex (Mhc) genes are believed to play a key role in the genetic basis of disease control. Although numerous studies have sought links between Mhc and disease prevalence, many have ignored the ecological and epidemiological aspects of the host-parasite interaction. Consequently, interpreting associations between prevalence and Mhc is difficult, while discriminating alleles for qualitative resistance, quantitative resistance and susceptibility remains challenging. Moreover, most studies to date have quantified associations between genotypes and disease status, overlooking the complex relationship between genotype and the properties of the Mhc molecule that interacts with parasites. Here, we solve these problems and demonstrate malaria parasite species-specific associations with functional properties of Mhc molecules in a wild bird population; effects that depend crucially on understanding the impacts and spatial epidemiology of these parasites. Furthermore, we demonstrate common functional properties of malaria-resistance alleles in passerines, suggesting this is a model system for parasite-Mhc associations in the wild.

Roseanne Miller
University of Aberdeen
Ecology Department
United Kingdom

Mate choice, multiple mating and MHC variation in sea trout (Salmo trutta)

poster 

Author(s): Miller, RJ, Martin, SA, Youngson, AF, Piertney, SB

Summary:

Understanding the factors that affect spatio-temporal levels and distribution of genetic diversity is essential for the management of genetic resources in natural populations. Traditionally, neutral markers have been utilised to examine the extent of migration-drift equilibrium within populations, but this ignores how sexual selection and plasticity in life strategy can influence patterns of adaptive genetic diversity that may directly influence individual fitness and population viability. Here we examine how MHC variation is maintained by mate choice decisions and multiple paternity in a population of sea trout in NE Scotland. Parentage of 1519 S. trutta offspring from 72 nests was characterised using ten microsatellite loci and one MHC-linked minisatellite locus. The level of multiple paternity was examined within and among nests and both sexes were found to practice multiple mating, with females mating with up to 11 males per nest and males with up to eight females. The level of amino acid dissimilarity among MHC alleles between consort and non-consort males was assessed and the overall levels of MHC diversity within nests under different mating scenarios was quantified to examine how extra pair paternity influences overall brood diversity. Multiple paternity is likely to increase genetic variation in a female’s offspring therefore maximising the chances that some offspring will be genetically equipped to deal with selective pressures. This bet hedging strategy may be pronounced in species, such as salmonids, which produce large broods, have high mortality rates in their first year, and spawn in their natal breeding grounds, which may heighten the risk of inbreeding. Mate choice towards consort males may enhance the chances of producing viable offspring as a more direct mechanism of estimating ‘good genes’.

Aleksandra Biedrzycka
Institute of Nature Conservation, Polish Academy of Sciences
Poland

Next Generation Sequencing reveals high complexity of the Major Histocompability Complex class I exon 3 in sedge warbler

poster 

Author(s): Biedrzycka, A, Radwan, J, Westerdahl, H

Summary:

The major Histocompability Complex (MHC) class I genes have received a considerable of interest from evolutionary biologists. Their role in parasite recognition and extreme polymorphism makes these genes a paradigm for studying genetic effects on survival, mate choice and pathogen resistance. Exon 3 of MHC class I genes encodes a part of the domain that binds and presents peptides from pathogens. Species possessing many highly polymporphic MHC loci are potentially under strong natural selection from parasites. Determining selection acting on MHC in natural population of such species over extended periods of time offers a great opportunity to reveal mechanisms maintaining MHC diversity. Here we present initial characterization of MHC class I genes diversity in a sedge warbler Acrocephalus schoenobaenus from population inhabiting natural wetlands in the Nida valley, SE Poland. We designed primers and determined diversity at MHC class I exon 3 both in cDNA and gDNA of 4 unrelated individuals with use of Next Generation Sequencing methods. We found extreme diversity at the MHC class I exon 3 of the sedge warbler. This data will be used for designing specific primers amplifying functional alleles of MHC class I exon 3 in sedge warbler. Subsequently, we are going to infer long-term selection on MHC class I in the species.

Julien Goebel
University of Lausanne
Department of Ecology and Evolution
Switzerland

Phylogenetic origin of the avian MHC class IIB

poster 

Author(s): Goebel, J, Burri, R, Promerová, M, Fumagalli, L

Summary:

The major histocompatibility complex (MHC) multigene family encodes genes involved in the vertebrates’ adaptive immune response. The exceptional evolutionary dynamics of MHC genes, including high rates of gene duplication and recombination, qualifies them as an ideal system to understand multigene family evolution. Mammalian MHCIIB paralogs evolve independently and their duplication history can commonly be traced back over tens of millions of years. Recent studies on birds report also strong evidence for the persistence of two ancient MHC class IIB lineages over at least 100 million years. At odds with this result, only few species studied so far appear to have retained both MHCIIB lineages, and it is unclear whether they have gone largely undetected, or whether they have been lost at high frequency. In the present study we therefore isolated MHCIIB genes from species all over the avian phylogeny. We aim at reconstructing the phylogenetic history of avian MHCIIB in order to provide an accurate estimate for the time of origin of the two ancestral avian MHCIIB lineages and estimate the rates of gene loss in each lineage. Qualitative results show that the two avian MHCIIB lineages evolved prior to the evolution of extant birds, and suggest the action of generally high, but strongly variable and phylogenetically unconstrained rates of concerted evolution in the avian MHCIIB. Thereby the present study provides important insights into the avian MHCIIB long-term evolutionary history and thus provides new information in unprecedented details about the evolution of an enigmatic multigene family.

Contacts

Chairman: Octávio S. Paulo
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Address

XIV Congress of the European Society for Evolutionary Biology

Organization Team
Department of Animal Biology (DBA)
Faculty of Sciences of the University of Lisbon
P-1749-016 Lisbon
Portugal

Website

Computational Biology & Population Genomics Group 
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