School of Biological and Chemical Sciences
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.
Department of Biology
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.
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.
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.
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.
Department of Biology
Horizontal gene transfer is an innovative mechanism in asexual eukaryotes to acquire novel functions
Author(s): Van Doninck, K, Danchin, EGJ, Flot, J
Asexuality is considered an evolutionary dead-end for metazoans, but bdelloid rotifers challenge this view as they are assumed to have persisted asexually for millions of years. Neither male sex organs nor meiosis have ever been observed in these microscopic animals. Females form oocytes through two successive mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing. In addition, bdelloids are able to survive extreme desiccation at any stage in their life cycle. Supporting long-term absence of meiosis and sexual reproduction, the genome architecture of the bdelloid rotifer Adineta vaga presents a high level of shuffling and rearrangement incompatible with conventional meiosis. Using an alien index approach, 8% of protein-coding genes in the A. vaga genome are probably of non-metazoan origin. Confirming this abundance of genes of non-metazoan origin, it has been estimated that at least 8% of the genes in Adineta ricciae, a related bdelloid species, are of foreign origin. This suggests that horizontal gene transfers (HGT) happen in bdelloids far more often than in other eukaryotes studied so far. For instance, this is twice the proportion observed in root-knot nematodes (3-4% of foreign genes) that were considered as holding the record for metazoan animals. In these nematodes, HGT have been shown to play an important role in the emergence of plant parasitism. In A. vaga, gene families involved in resistance to oxidation and carbohydrate metabolism, essential for desiccation resistance, are significantly expanded and many have been acquired through HGT. Quantitative PCR studies confirm the expression of foreign genes related to desiccation resistance in the bdelloid species A. vaga. Whether acquisition of foreign genes via HGT is a key innovative mechanism in eukaryotes allowing adaptation to changing environments in the absence of sexual reproduction is an important question that deserves further investigation.
Dpt "Genomes and Genetics"
Molecular tinkering of nanomachines: the evolution of a direct protein delivery system from the bacterial flagellum
Author(s): Abby, S, Rocha, EPC
Protein secretion systems drive bacterial virulence, symbiosis and competition. Some components are homologous between systems and/or with other cellular appendages. This suggests extensive evolutionary tinkering of the molecular components of secretion systems and other complex cellular membrane machineries. Here, we present a scenario for the evolution of the non-flagellar type 3 secretion system (NF-T3SS). This system allows the direct injection of proteic effectors into eukaryotic cells, and is involved in both beneficial (symbiosis) and antagonist (pathogenicity) relationships between bacteria and eukaryotes. This system is partly homologous to the bacterial flagellum. We developed tools to detect NF-T3SS in genomes, and used phylogenomics and comparative genomics to study the evolution of this system. We could show that NF-T3SS derived from a flagellar ancestor in a series of steps, each representing accretions to the system of proteins from other molecular machines. This resulted in a secretion system that diversified and adapted to different types of hosts and ecological associations. We also found a new intermediate conserved system in myxococcales, which emerged from the ancestral NF-T3SS and is neither a direct protein delivery system nor a flagellum. Thus secretion systems have intricate histories. This study and ongoing work should help deciphering the common evolutionary history of different secretion systems. It also provides clues on patterns of evolution of the large molecular structures that drive ecological interactions.
Swiss Institute for Experimental Cancer Research
Origins and functional evolution of long non-coding RNAs in tetrapods
Author(s): Necsulea, A, Soumillon, M, Liechti, A, Daish, T, Grutzner, F, Kaessmann, H
The search for molecular evolutionary innovations strongly relies on comparative analyses of gene repertoires, sequences and expression patterns. Such studies have been instrumental for our understanding of the genetic basis of lineage-specific phenotypes and of individual gene functions. However, these analyses have so far been restricted to protein-coding genes, and the contribution of other categories of genes, such as long noncoding RNAs (lncRNAs), has yet to be explored. Here, we use RNA sequencing to identify lncRNAs in eleven tetrapod species and we present the first large-scale evolutionary study of lncRNA repertoires and expression patterns. We identify ~11,000 primate-specific lncRNA families, which show evidence for selective constraint during recent evolution. These “young” lncRNA genes are lowly transcribed and predominantly expressed in testes, in agreement with the hypothesis that the permissive chromatin state of the testis favors the emergence of new genes. Interestingly, we also identify ~2,400 highly conserved lncRNAs, including ~400 genes that likely originated more than 300 million years ago. We find that lncRNAs, in particular ancient ones, are generally actively regulated and may predominantly function in embryonic development. Most lncRNAs evolve rapidly in terms of sequence and expression levels, but global patterns like tissue specificities are often conserved. We compared expression patterns of homologous lncRNA and protein-coding families across tetrapods to reconstruct an evolutionarily conserved co-expression network. This network, which surprisingly contains many lncRNA hubs, suggests potential functions for lncRNAs in fundamental processes like spermatogenesis or synaptic transmission, but also in more specific mechanisms such as placenta growth suppression through miRNA production.
The paradigma of irreversibility in gametophytic self-incompatibility: the Malus and Prunus systems
Author(s): Vieira, CP, Aguiar, B, Vieira, J, Cunha, AE, Iezzoni, A, VanNocker, S
In the present hypothesis, S-RNase-based gametophytic self-incompatibility (GSI) evolved once before the split of the Asteridae and Rosidae, but the Rosaceae Malus and Prunus GSI systems are different: in Prunus the S-RNase gene presents two introns and the S-pollen is a single F-box gene (called SFB). The two genes show evidence for a partially coevolved history, both presenting high levels of synonymous and non-synonymous divergence, as well as positively selected amino acid sites that account for the specificities present in natural populations. In Malus, the S-RNase gene has one intron, and multiple S-pollen F-box genes (called SFBBs) have been described. Levels of diversity at the S-RNase gene are 10 times higher than at the SFBB genes. Nevertheless, intra-haplotypic diversity of SFBB is similar to the S-RNase gene. Moreover, there is evidence for amino acids under positive selection only when intra-haplotype SFBB genes are analyzed. Thus, it is not surprising that different self-recognition mechanisms have been proposed: in Prunus self S-RNases are protected from degradation by the self-SFB protein, while in Malus each SFBB protein is predicted to interact with a subset of non-self S-RNases that mediates their degradation. Here, we perform a detailed characterization of S-RNase and F-box like genes present in the P. persica and M. domestica genomes. Phylogenetic analyses revealed three duplications that predate Malus and Pyrus speciation. The gene lineage determining GSI function are different in Malus and Prunus. Expression analyses in 12 Malus tissues revealed that two of the S-RNase lineage genes are expressed mostly in pistils, but one has acquired seed expression. In Malus the closest SFB-like gene shows the highest expression in stamen but is also expressed in seeds. An hypothesis for the evolution of Malus and Prunus GSI is presented. Implications of the polyphyletic S-RNase GSI evolution on uncharacterized GSI systems are discussed.
The rapid life cycle of Drosophila orphans
Author(s): Schlötterer, C, Palmieri, N, Nolte, V, Kosiol, C
Orphans are genes restricted to a single phylogenetic lineage. They emerge at high rates and frequently provide a selective advantage or even essential functions to their host. While these features predict an accumulation of genes, the gene number has remained remarably constant through evolution. This paradox of a stable gene number in the presence of a high rate of gene birth has not been resolved. Because orphan genes were mainly analyzed over large evolutionary time scales, orphan loss, a key factor of orphan evolution, remained unexplored. Here, we study the patterns of orphan turnover among close relatives in the Drosophila obscura group. We show that orphans are not only emerging at a high rate, but they are also rapidly lost. The pattern of orphan loss is clearly non-random: young orphans are more likely to be lost than orphans, which originated earlier. Furthermore, highly expressed orphan genes with a strong male-bias are more likely to be retained. Since lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that intron loss is not driven by different evolutionary rates, but lineage specific functional requirements.