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Kohtaro Tanaka
Instituto Gulbenkian de Ciência

cis-regulatory evolution and functional diversification of gene duplicates in Diptera


Author(s): Tanaka, K, Hazbun, A, Vreede, B, Diekmann, Y, Roch, F, Sucena, É


Gene duplication plays a major role in evolution of novel gene functions as it provides a material basis for variation and selection. We are interested in elucidating how cis-regulatory changes contribute to functional diversification ensuing gene duplication. To address this question we are studying the Three-Finger-Domain Protein/Ly6 gene family in insects. Members of this family encode different GPI-anchored membrane proteins and are fully conserved across drosophilids. Our analyses of the sequenced insect genomes indicate that a subset of these genes is unique to higher dipterans. We are focusing our attention on seven paralogues of Drosophila, which our phylogenetic analysis showed to derive from sequential duplications of a single orthologue. In order to determine how their expression domains diversified, we have characterized the embryonic expression patterns of the Drosophila paralogues and their unduplicated orthologues in other insects representing different phylogenetic positions and stages of duplication (the Mediterranean fruit fly, Ceratitis capitata, the scuttle fly, Megaselia abdita, the mosquito, Anopheles, the butterfly, Bicyclus anynana and the red flour beetle, Tribolium castaneum). We found that the original expression domain of the unduplicated orthologue localized predominantly to the developing nervous system, which, upon subsequent duplications, expanded to a wide array of tissues. While a subset of the duplicates retained the tissue-specificity of the unduplicated orthologues, the others acquired novel tissue-specific expression suggesting neofunctionalization. We are currently identifying the cis-regulatory elements of the duplicates and the unduplicated orthologues to elucidate the cis-regulatory mechanisms underlying the evolution of divergent expression patterns.

Yannick Wurm
Queen Mary University London
School of Biological and Chemical Sciences
United Kingdom

AY-like social chromosome causes alternative colony organization in fire ants


Author(s): Wurm, Y, Wang, J, Nipitwattanaphon, M, Riba-Grognuz, O, Huang, Y, Shoemaker, D, Keller, L


Intraspecific variability in social organization is common, yet the underlying causes are rarely known. In the fire ant Solenopsis invicta, the existence of two divergent forms of social organization is under the control of a single Mendelian genomic element marked by two variants of an odorant-binding protein gene4–8. Here we characterize the genomic region responsible for this important social polymorphism, and show that it is part of a pair of hetero- morphic chromosomes that have many of the key properties of sex chromosomes. The two variants, hereafter referred to as the social B and social b (SB and Sb) chromosomes, are characterized by a large region of approximately 13 megabases (55% of the chromosome) in which recombination is completely suppressed between SB and Sb. Recombination seems to occur normally between the SB chromo- somes but not between Sb chromosomes because Sb/Sb individuals are non-viable. Genomic comparisons revealed limited differenti- ation between SB and Sb, and the vast majority of the 616 genes identified in the non-recombining region are present in the two variants. The lack of recombination over more than half of the two heteromorphic social chromosomes can be explained by at least one large inversion of around 9 megabases, and this absence of recombination has led to the accumulation of deleterious mutations including repetitive elements in the non-recombining region of Sb compared with the homologous region of SB. Importantly, most of the genes with demonstrated expression differences between indi- viduals of the two social forms reside in the non-recombining region. These findings highlight how genomic rearrangements can maintain divergent adaptive social phenotypes involving many genes acting together by locally limiting recombination.

Lene Martinsen
Harvard University/Oslo University
Department of Organismic and Evolutionary Biology
United States

Are there patterns in the formation and expression of novel genes?


Author(s): Martinsen, L, Ponce, R


Observed differences between species are often due to differences at genomic level. In particular, the analysis of newly evolved genes provides information that helps us to understand the evolution of novel functions. Here, we examine the mechanisms involved in the formation of novel genes (less than 50 MYA) and we characterize the expression patterns of these genes. This illustrates the variety of mechanisms implicated in the formation of new genes, as well as the preferential location of expression of novel functions. We further analyze the Sdic gene family and use it to investigate in greater detail the formation and expression of novel genes. The Sdic gene family, a young gene family in Drosophila melanogaster, represents an interesting window into the evolution of novel genes, as it evolved after the split of D. melanogaster and D. simulans i.e. less than 2 million years ago. This gene family originated from a formation of a chimera of two unrelated genes, that was followed by several duplication events, being therefore a candidate for the study of two important mechanisms of gene formation: gene shuffling and duplication. This family is composed by several tandem copies of the gene Sdic, and at least one copy (sdic1) is expressed in testis, incorporated into the sperm tail and encodes a sperm specific intermediate chain. It has recently been showed that although this novel gene is not essential for the development of spermatids and Sdic knock-out males are fertile with no effect on the size or sex ratio of their progeny, Sdic has a role on sperm competition. This effect of Sdic in improving sperm competition suggests that Sdic may have had an important role, contributing to the species barrier between D. melanogaster and D. simulans. The analysis of particular newly evolved genes provides information in finer detail, that we hope can be generalized and will help understand the evolution of new genes and new functions in the genomes.

Vaishali Katju
University of New Mexico
Department of Biology
United States

Copy-number changes in experimental evolution: rates, fitness effects and adaptive significance


Author(s): Katju, V


Gene copy-number differences due to gene duplications and deletions are rampant in natural populations and play a crucial role in the evolution of genome complexity. The rate at which new gene copies appear in populations greatly influences their evolutionary dynamics and standing gene copy-number variation in populations. The duplication rate may therefore have profound effects on the role of adaptation in the evolution of duplicated genes with important consequences for the evolutionary potential of species.

In this talk, I will discuss three long-term experimental evolution experiments in Caenorhabditis elegans that we have utilized to investigate fundamental properties of the gene duplication process. First, we conducted oligonucleotide array comparative genome hybridization (oaCGH) on C. elegans mutation accumulation (MA) lines subjected repeatedly to single-worm bottlenecks each generation to provide the first direct estimate of the spontaneous genome-wide rate of duplication in a multicellular eukaryote. The gene duplication rate in C. elegans is quite high and exceeds the spontaneous rate of point mutation per nucleotide site in this species by two orders of magnitude. Second, I discuss new oaCGH results of low-fitness experimental lines subjected to adaptive recovery via population expansion to investigate whether copy-number variants (CNVs) constitute a common mechanism of adaptive genetic change during compensatory evolution. Lastly, long-term spontaneous MA lines maintained at three varying effective population sizes for >400 generations were used to investigate whether CNVs accumulate differentially under varying intensities of natural selection and provide some insights into their average fitness effects.

Richard Cordaux
CNRS / Université de Poitiers
UMR 7267 Ecologie et Biologie des Interactions

Evolutionary innovations in sex determination mechanisms driven by Wolbachia bacterial endosymbionts in the isopod Armadillidium vulgare


Author(s): Cordaux, R, Badawi, M, Grève, P, Giraud, I, Ernenwein, L, Leclercq, S


In the isopod Armadillidium vulgare, genetic sex determination follows female heterogamety (ZZ males and ZW females). However, many A. vulgare populations harbor maternally-inherited Wolbachia bacterial endosymbionts which can convert genetic males into phenotypic females, leading to populations with female-biased sex ratios (1). The W sex chromosome has been lost in lines infected by Wolbachia and all individuals are ZZ genetic males. The female sex is determined by the inheritance of Wolbachia by the A. vulgare individual, thereby leading to a shift from genetic to cytoplasmic sex determination. We are using comparative genomics and expression profiles to identify Wolbachia gene(s) responsible for feminization of A. vulgare males. Surprisingly, some A. vulgare lines exhibit female-biased sex ratios despite the lack of Wolbachia. In these lines, female individuals are ZZ genetic males carrying an unknown feminizing factor. To elucidate the genetic basis of female sex determination in these lines, we sequenced the genome of a female by illumina. We identified a large piece of the Wolbachia genome transferred to the A. vulgare nuclear genome. The transferred genomic fragment shows non-Mendelian inheritance and co-segregates perfectly with the female sex in pedigrees, in agreement with observed biased sex ratios. These results suggest that sex determination in these A. vulgare lines is under the control of nuclear gene(s) of bacterial origin. Overall, our results indicate that Wolbachia bacteria can drive shifts in sex determination mechanisms in A. vulgare. More generally, they emphasize that bacterial endosymbionts can be powerful sources of evolutionary novelty for fundamental biological processes in eukaryotes, such as sex determination. This research is funded by an ERC Starting Grant (EndoSexDet) to RC.

(1) Cordaux et al. (2011) The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends in Genetics. 27, 332-341.

Raquel Ruivo
CIIMAR, University of Porto

Evolutionary study of RDH10 gene family reveals a novel member retained in ectothermic vertebrates


Author(s): Ruivo, R, Lopes-Marques, M, Santos, MM, Castro, LC


Nuclear receptor-mediated retinoic acid signalling is crucial for organ modelling and maintenance. Active retinoid biosynthesis involves a two-step oxidation cascade: retinol oxidation followed by retinaldehyde dehydrogenase activity, suggested to coordinate retinoic acid supply. Recent studies have highlighted the functional role of a membrane-associated retinol dehydrogenase (RDH10) in the first oxidation step in mammals. This enzyme displays tissue and time-specific expression patterns that correlate with both retinoic acid and retinaldehyde dehydrogenase activities: suggestive of an additional checkpoint for retinoic acid regulation. Here we investigated the evolution of chordate rdh10. While a single copy, rdh10a, is observed in birds and mammals, reptiles, amphibians and teleosts exhibit an additional uncharacterized gene, rdh10b. Both rdh10a and rdh10b have duplicate copies in teleosts. Phylogenetic and paralogy analysis revealed that vertebrate rdh10a and rdh10b resulted from whole genome duplication in stem vertebrate evolution; interestingly, with significant functional divergence amongst paralogues. Following duplication, rdh10b was lost in warm-blooded lineages and retained in cold-blooded animals. Both enzymes exhibit conserved reaction cores and tri-dimensional folding; yet, the membrane-association designs appear different: unlike RDH10A, topology predictions advocate for RDH10B solubility. Also, a unique negatively charged insertion is observed in RDH10A isoforms. Gene expression patterns in teleosts, D. rerio and O. nicotilus, were also examined. While rdh10a is ubiquitously expressed, rdh10b expression is typically restricted to gonads, skin, and brain, and is concomitant with the onset of pigmentation and circulation during teleost embryonic development. Together these results support a functional specialization within the rdh10 family and emphasize a dichotomy among vertebrates according to thermal homeostasis mechanisms.

Ariel Chipman
The Hebrew University of Jerusalem
Ecology, Evolution & Behavior

Evolutionary “tinkering” in the origin of the insect terminal patterning system


Author(s): Chipman, AD, Weisbrod, A


A key early process in development is the determination of the embryonic axes. The anterior-posterior axis in insects is determined by a series of signaling pathways and transcription factors. These are best known from the fruitfly Drosophila melanogaster, where the torso pathway activates a number of posterior transcription factors, while interacting diffusible factors define the anterior. We have cloned the homologues of most of the key players in terminal patterning from the milkweed bug Oncopeltus fasciatus, focusing on huckebein, torsolike, hunchback, orthodenticle and tailless. We then studied their expression and function, and their interaction with other early developmental pathways. Our results show that many of the pathways known to be involved in Drosophila terminal patterning have different roles in Oncopeltus development. We suggest that their roles in Drosophila are derived from the more ancestral roles still preserved in Oncopeltus. We use our results to discuss a model for the evolution of the terminal patterning system in insects, and show that the evolution of this pathway is a classic example of evolutionary "tinkering", where different elements are co-opted independently into a single novel patterning system.

Pierrick Labbé
University of Montpellier 2
Institute for Evolutionary Sciences

Gene duplications: a role in adaptive evolution


Author(s): Labbé, P, Milesi, P, Weill, M, Lenormand, T


Evolutionary potential is limited by the number and type of genes present, but how these limits shape the evolution of new functions remains a matter of debate. In this context, gene duplications are thought to be the main source of raw material for new evolutionary features: duplications are essentially envisioned as genomic substrates for long-term adaptation. Their early evolution is thus often neglected, notably how gene-dosage modifications affect fitness and condition their first steps. The evolution of insecticide resistance in the mosquito Culex pipiens is one of the few examples of contemporary duplications. Resistance represents a genetic adaptation to the environmental changes induced by insecticides, and as such, provides evolutionary biologists with a contemporary model for studying parameters that influence ongoing adaptation. The ace-1 gene encodes the acetylcholinesterase (AChE1), the target of organophosphate (OP) insecticides. A mutation in this gene causes high resistance levels in many mosquito species. However, a strong genetic constraint drives resistance evolution, as the degree of resistance and the ability to degrade ACh trade off. Recently, we identified in Cx. pipiens new ace-1 alleles that carry one susceptible and one resistant copy associated on the same chromosome. These different duplicated alleles show different dynamics in the field. We propose that duplications are selected to disentangle the two functions, i.e., by improving synapse signaling and mosquito’s fitness while maintaining resistance. I will present our recent work investigating 1) the duplication origin at the molecular level and 2) the complex gene-dosage/fitness relations and their impact in the field dynamics of these innovations. Our work stresses the role of duplications as immediate adaptive features, but shows that their fate is checked by natural selection early on: only those passing its short-term sieve can become seeds for future evolution.

Antoine Frénoy
Université Paris Descartes
Faculté de Médecine

Genetic architecture promotes the evolution and maintenance of cooperation: the evolutionary constraint of coding overlaps on functionally unrelated genes


Author(s): Frénoy, A, Taddei, F, Misevic, D


When cooperation has a direct cost and an indirect benefit, a selfish behavior is more likely to be selected for than an altruistic one. Kin and group selection do provide evolutionary explanations for the existence of stable populations of cooperators in nature, but we still lack the full understanding of the genomic mechanisms that can prevent cheater invasion. We used Aevol, an agent-based, in silico genomic platform to evolve populations of digital organisms that compete, reproduce, and cooperate by secreting a costly public good. We found that populations of phenotypically equal cooperating individuals often have very different abilities to resist cheater invasion. To understand the underlying mechanisms, we performed bio-inspired genomics analysis by determining and comparing the locations of metabolic and secretion genes, as well as the relevant promoters and terminators. We found that populations of cooperators characterized by the strong association between metabolic and secretion genes (promoter sharing, overlap via frame shift or sense-antisense encoding) were more robust to cheater invasion than ones where such association was weak. We performed mutation analysis of the evolved individuals and determined that the accessibility of mutations decreasing cooperation without decreasing overall fitness was negatively correlated with the amount of operons and overlap between secretion and metabolism. Effectively, cooperation evolved to be protected and robust to mutations through overlapping genetic architecture, especially when cooperation was costly. Due to operon sharing and gene overlap, even when mutations that eliminate cooperation appear, they are likely to be selected against due to their simultaneous and direct negative effect on fitness. Our results uncover an important genetic mechanism for the evolution and maintenance of cooperation, and suggest promising methods for preventing loss of genes introduced into biological synthetic organisms.

Sanne Nygaard
University of Copenhagen

Genomic changes during the evolution of increasing specialization in fungus-farming ants


Author(s): Nygaard, S, Li, C, Schiøtt, M, Zhang, G, Xiao, J, Meng, X, Wang, J, Boomsma, JJ


Ants are an ecologically important group of insects with a vast array of specialized lifestyles and symbioses. One of the most spectacular ant symbioses is fungus farming, found in a single clade of New World (attine) ants, a mutualism to which the ants contribute plant material in exchange for food provided by the fungal crops. Since this mutualism evolved in the Amazon basin from hunter-gatherer like ancestors some 50 mya, it has undergone a series of evolutionary transitions of which the use of specialized rather than generalist fungal strains, active herbivory rather than using dead plant parts, polymorphic rather than monomorphic worker castes, and multiple rather than single mating of queens are the most important. The advent of high-throughput sequencing techniques now allows these questions to also be addressed at the molecular evolutionary level. In a recent study, we showed that the genome sequence of the leafcutter ant Acromyrmex echinatior, a representative of the most highly derived leaf-cutting fungus-farming ants, has characteristic changes in detoxification pathways, loss of function in arginine metabolism pathways, and expansion of specific peptidase gene-families relative to other ant genomes. We have now sequenced and partly analyzed the genomes of five additional fungus-farming ant species, representing all phylogenetic branches of the higher attine ants and a lower attine outgroup, and thus most of the major evolutionary transitions. These comparative genomic analyses allow us to assess rates of gains and losses of genes and variation in lineage-specific selective pressures, differences that we hope to connect to some of the phenotypic adaptations in the respective lineages.


Chairman: Octávio S. Paulo
Tel: 00 351 217500614 direct
Tel: 00 351 217500000 ext22359
Fax: 00 351 217500028


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


Computational Biology & Population Genomics Group