Evolution of a supergene that regulates a trans-species social polymorphism

Supergenes are clusters of linked genetic loci that jointly affect the expression of complex phenotypes, such as social organization. Little is known about the origin and evolution of these intriguing genomic elements. Here we analyse whole-genome sequences of males from native populations of six fire ant species and show that variation in social organization is under the control of a novel supergene haplotype (termed Sb), which evolved by sequential incorporation of three inversions spanning half of a 'social chromosome'. Two of the inversions interrupt protein-coding genes, resulting in the increased expression of one gene and modest truncation in the primary protein structure of another. All six socially polymorphic species studied harbour the same three inversions, with the single origin of the supergene in their common ancestor inferred by phylogenomic analyses to have occurred half a million years ago. The persistence of Sb along with the ancestral SB haplotype through multiple speciation events provides a striking example of a functionally important trans-species social polymorphism presumably maintained by balancing selection. We found that while recombination between the Sb and SB haplotypes is severely restricted in all species, a low level of gene flux between the haplotypes has occurred following the appearance of the inversions, potentially mitigating the evolutionary degeneration expected at genomic regions that cannot freely recombine. These results provide a detailed picture of the structural genomic innovations involved in the formation of a supergene controlling a complex social phenotype

Akazien-bewohnende Pseudomyrmex Ameisen - Integration physiologischer, verhaltensbiologischer, chemischer und genetischer Daten zur Untersuchung der Stabilität von Ameisen-Pflanzen Mutualismen

Mutualisms are interspecific interactions that benefit all partners involved. These interactions often include reciprocal adaptations of the partners. Acacia ant-plants secrete sucrose-free extrafloral nectar and I demonstrated that the defending Pseudomyrmex ant mutualists correspondingly almost completely lacked invertase activity (15 to 19 ng glucose released µg-1 ant fresh weight min-1). In contrast, generalist and exploiting ant species possessed invertase activity (89 to 107 ng glucose µg-1 min-1). In experiments, sucrose uptake induced invertase activity in generalist (300%) and exploiting workers (250%) as well as in larvae of all species (170-310%) investigated, but not in mutualist workers. Thus, the mutualists loose invertase during their ontogeny. This reduced metabolic capacity ties the mutualists to their host plants, but it does not prevent the mutualism from exploitation. A molecular phylogeny demonstrated that the exploiter species did not evolve from former mutualists but from generalists. Thus, being physiologically specialized and dependent on their host plants prevents mutualists from evolving into exploiters, while other mechanisms are required to stabilize a mutualism against the exploitation by species that evolved from generalists. The colonization patterns of a mutualistic and a parasitic acacia-inhabitant were compared using three complementary approaches: observations of aggression behavior, chemical analyses of cuticular hydrocarbon profiles and genetic microsatellite analyses. Genetic data indicated that one colony of the mutualist Pseudomyrmex ferrugineus inhabited up to two host plants (ø 1.56), while several parasitic P. gracilis colonies (ø 2.23) shared the same individual host. In both species, ant individuals inhabiting the same acacia possessed characteristic chemical profiles. In behavioral experiments under field conditions, inhabitants sharing the same acacia showed no aggression, which is in line with cuticular hydrocarbon profiles. Genetic, chemical and behavioral patterns were concordant for P. ferrugineus, while genetic heterogeneity and low relatedness (Rmin=0.00±0.18) of P. gracilis was in contradiction to chemical and behavioral data. The non-aggressive coexistence of different colonies of P. gracilis seems to prevent the inhabitation of hosts by other species. Genetic identity of ant colonies, the ants’ chemical profiles and their behavior towards conspecifics shape the colonization pattern of acacias and can determine the outcome of plant-ant interactions. Large and fast growing colonies are advantageous in competitive environments to allow for efficient nest defense and foraging. How the obligate acacia-ant Pseudomyrmex peperi forms colonies was investigated in the present study. The species establishes distinct, but highly polygynous colonies that can inhabit large clusters of host trees. Analyzing workers, males, queens and virgin queens (264 individuals) from two supercolonies with eight polymorphic microsatellite markers indicated that colonies are founded by one singly mated queen and supercolonies are established by intranidal mating among colony-derived males with daughter queens. This allows colonies to constantly grow by budding without having to found new colonies. Ancestral states reconstruction revealed that polygyny represents the derived state among acacia-ants and has evolved at least twice independently. The extreme polygyny of Pseudomyrmex peperi achieved by intranidal mating may play an important role for species coexistence in a dynamic and competitive habitat. I was able to identify physiological, genetic and behavioral adaptations of mutualistic acacia-ants to their specific life style. Large colonies with high numbers of individuals, which allow for efficient host defense, seem to be a key adaptation of mutualistic acacia-ants. Constant colony growth is possible especially in the polygynous acacia-ant Pseudomyrmex peperi and seems to be a higher adaptation towards the life style as acacia-inhabitant. High relatedness among individuals colonizing the same host reduces conflicts and increases inclusive fitness of the individuals. The genes and consequently the behavior of the mutualist workers are then passed on to the next generation and allow the mutualism to persist in evolutionary terms. In contrast, ant species that parasitize the mutualism of acacias were not adapted to their hosts. They do not depend on the host plant and decrease plant fitness. These parasites can only persist in evolutionary terms because they coexist with mutualistic ant species that assure the maintenance of myrmecophytic traits in host plant populations.Mutualismen sind Interaktionen verschiedener Arten zu gegenseitigem Nutzen. Diese Wechselbeziehungen können Anpassungen der Partner einschließen. Als eine solche gegenseitige Adaptation sezernieren Ameisenakazien Saccharose-freien extrafloralen Nektar (EFN) und die auf den Pflanzen lebenden mutualistischen Ameisenarten haben in Anpassung an ihre Wirtspflanze die Fähigkeit verloren, das Enzym Invertase zur Spaltung von Saccharose zu expremieren. Zudem konnte experimentell gezeigt werden, dass die Aufnahme von Saccharose die Invertase-Aktivität von parasitischen (250%) und generalistischen (300%) Ameisenarten erhöht, nicht aber die von Mutualisten. Im Gegensatz zu adulten Tieren zeigten Larven aller drei untersuchten Ameisengruppen eine induzierbare Invertase-Aktivität (170-310%). Diese während ihrer Ontogenese reduzierte Verdauungskapazität bindet die mutualistischen Ameisenarten physiologisch an ihren Wirt. Andererseits verhindert jedoch der Verlust von Saccharose im EFN nicht die Ausbeutung des Mutualismus durch parasitische Ameisenarten. Anhand einer molekularen Phylogenie basierend auf DNA-Sequenzen wurde nachgewiesen, dass die Parasiten aus generalistischen Arten evolviert sind und nicht aus Mutualisten. Die physiologische Anpassung und die damit einhergehende Abhängigkeit der mutualistischen Ameisen von ihrer Wirtspflanze scheint die Evolution zu einem Parasiten zu verhindern, nicht aber die Ausbeutung des Systems durch Parasiten, welche aus Generalisten evolviert sind. Die Koloniestruktur mutualistischer und parasitischer Ameisenarten wurde in der vorliegenden Arbeit mit Hilfe von Verhaltensbeobachtungen, chemischen Analysen kutikulärer Kohlenwasserstoffe und genetischen Mikrosatelliten-Daten vergleichend untersucht. Verwandtschaftsanalysen belegten, dass eine Kolonie des Mutualisten P. ferrugineus bis zu zwei (ø 1.56) Akazien-Pflanzen besiedelte, wohingegen sich mehrere Kolonien des Parasiten P. gracilis (ø 2.23) einzelne Wirtspflanzen teilten. Bei beiden Arten besaßen die Individuen, welche dieselbe Wirtspflanze bewohnten, charakteristische Profile kutikulärer Kohlenwasserstoffe. In Verhaltensexperimenten im Freiland zeigten die Bewohner einer Wirtspflanze keine Aggressivität untereinander, was durch die Profile der kutikulären Kohlenwasser-stoffe erklärt werden konnte. Genetik, Chemie und Verhalten von P. ferrugineus wiesen somit ähnliche Muster auf, während bei P. gracilis die genetische Heterogenität und der z.T. geringe Verwandtschaftsgrad (Rmin=0.00±0.18) im Widerspruch zu Chemie und Verhalten standen. Durch die friedliche Koexistenz verschiedener Kolonien des Parasiten P. gracilis kann der limitierte Lebensraum „Akazie“ vor Besiedelung durch artfremde, konkurrierende Ameisen geschützt werden. Die Interaktion zwischen Ameisen und Pflanzen hat also Einfluss auf die genetische Identität von Ameisenkolonien, ihre chemischen Profile und ihr Verhalten gegenüber koloniefremden Artgenossen. In einem kompetitiven Habitat sind große und schnell wachsende Kolonien von Vorteil, weil diese eine besonders effiziente Futtersuche und Nestverteidigung ermöglichen. In der vorliegenden Arbeit wurde untersucht, mit welchen Strategien die mutualistische Ameisenart Pseudomyrmex peperi Kolonien etabliert. Es konnte gezeigt werden, dass die Art extrem polygyne Kolonien bildet und so große Gruppen von Wirtspflanzen besiedelt. Mikrosatelliten-Daten zeigten, dass — trotz der großen Anzahl von Königinnen — Kolonien von einer einmal verpaarten Königin gegründet werden und durch Tochterköniginnen, welche mit Männchen aus derselben Kolonie verpaart sind, zu Superkolonien heranwachsen. Basierend auf DNA-Sequenzdaten wurde gezeigt, dass Polygynie innerhalb der mutualistischen Akazien-Ameisen das abgeleitete Merkmal darstellt. Die Polygynie von P. peperi ermöglicht es der Art, eine langjährige Beziehung mit ihrer Wirtspflanze einzugehen. Diese Sozialstruktur scheint eine weiterführende Anpassung der Ameisenart an ihre Wirtspflanze zu sein. In der vorliegenden Arbeit konnten physiologische, genetische sowie verhaltensbiologische Anpassungen mutualistischer Akazien-Ameisen an ihre Lebensweise identifiziert werden. Extreme Koloniegrößen mit hohen Individuenzahlen, welche ihre Wirtspflanze effektiv verteidigen, scheinen eine wichtige Anpassung von Akazien-Ameisen zu sein. Besonders polygyne Arten sind zu einem kontinuierlichen Koloniewachstum fähig. Durch einen hohen Verwandtschaftsgrad unter den Ameisen einer Akazie werden Konflikte reduziert und die Gesamtfitness der Individuen erhöht. Die Gene und daher das Verhalten der mutualistischen Ameisen wird somit an die nächste Generation weiter gegeben und ermöglicht ein Bestehen des Mutualismus in evolutionären Zeiträumen. Ameisen hingegen, die den Mutualismus parasitieren, sind nicht an die Wirtspflanze angepasst. Sie sind nicht von ihrer Wirtspflanze abhängig und reduzieren durch ihr Verhalten die Fitness der Pflanzen. Diese Parasiten können evolutionär nur bestehen, da sie mit den mutualistischen Arten coexistieren und letztere den Erhalt myrmekophytischer Eigenschaften der Wirtspflanzen gewährleisten

A Coverage Criterion for Spaced Seeds and its Applications to Support Vector Machine String Kernels and k-Mer Distances

Spaced seeds have been recently shown to not only detect more alignments, but also to give a more accurate measure of phylogenetic distances (Boden et al., 2013, Horwege et al., 2014, Leimeister et al., 2014), and to provide a lower misclassification rate when used with Support Vector Machines (SVMs) (On-odera and Shibuya, 2013), We confirm by independent experiments these two results, and propose in this article to use a coverage criterion (Benson and Mak, 2008, Martin, 2013, Martin and No{\'e}, 2014), to measure the seed efficiency in both cases in order to design better seed patterns. We show first how this coverage criterion can be directly measured by a full automaton-based approach. We then illustrate how this criterion performs when compared with two other criteria frequently used, namely the single-hit and multiple-hit criteria, through correlation coefficients with the correct classification/the true distance. At the end, for alignment-free distances, we propose an extension by adopting the coverage criterion, show how it performs, and indicate how it can be efficiently computed.Comment: http://online.liebertpub.com/doi/abs/10.1089/cmb.2014.017

A Coverage Criterion for Spaced Seeds and its Applications to Support Vector Machine String Kernels and k-Mer Distances

Spaced seeds have been recently shown to not only detect more alignments, but also to give a more accurate measure of phylogenetic distances (Boden et al., 2013, Horwege et al., 2014, Leimeister et al., 2014), and to provide a lower misclassification rate when used with Support Vector Machines (SVMs) (On-odera and Shibuya, 2013), We confirm by independent experiments these two results, and propose in this article to use a coverage criterion (Benson and Mak, 2008, Martin, 2013, Martin and No{\'e}, 2014), to measure the seed efficiency in both cases in order to design better seed patterns. We show first how this coverage criterion can be directly measured by a full automaton-based approach. We then illustrate how this criterion performs when compared with two other criteria frequently used, namely the single-hit and multiple-hit criteria, through correlation coefficients with the correct classification/the true distance. At the end, for alignment-free distances, we propose an extension by adopting the coverage criterion, show how it performs, and indicate how it can be efficiently computed.Comment: http://online.liebertpub.com/doi/abs/10.1089/cmb.2014.017

Relaxed selection underlies genome erosion in socially parasitic ant species

Inquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species. They have evolved many times convergently, are often evolutionarily young lineages, and are almost invariably rare. Focusing on the leaf-cutting ant genus Acromyrmex, we compared genomes of three inquiline social parasites with their free-living, closely-related hosts. The social parasite genomes show distinct signatures of erosion compared to the host lineages, as a consequence of relaxed selective constraints on traits associated with cooperative ant colony life and of inquilines having very small effective population sizes. We find parallel gene losses, particularly in olfactory receptors, consistent with inquiline species having highly reduced social behavioral repertoires. Many of the genomic changes that we uncover resemble those observed in the genomes of obligate non-social parasites and intracellular endosymbionts that branched off into highly specialized, host-dependent niches

Phylogeography of Pogonomyrmex barbatus and P. rugosus Harvester Ants: A Complex Regional History of Ancient Vicariance and Recent Expansion in Arid- Adapted Insects, and Implications for the Success of Cryptic Hybrid Lineages with GCD

abstract: Here I present a phylogeographic study of at least six reproductively isolated lineages of harvester ants within the Pogonomyrmex barbatus and P. rugosus species group. The genetic and geographic relationships within this clade are complex: four of the identified lineages are divided into two pairs, and each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because interlineage matings within each pair are the sole source of hybrid F1 workers; these workers build and sustain the colonies, facilitating the production of the reproductive caste, which results solely from intralineage fertilizations. This system of genetic caste determination (GCD) maintains genetic isolation among these closely related lineages, while simultaneously requiring co-expansion and emigration as their distributions have changed over time. Previous studies have also demonstrated that three of the four lineages displaying this unique genetic caste determination phenotype are of hybrid origin. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and plan future inquiries in a more complete historical biogeographic context. Using mitochondrial DNA sequences sampled across most of the morphospecies' ranges in the U.S. and Mexico, I employed several methods of phylogenetic and DNA sequence analysis, along with comparisons to geological, biogeographic, and phylogeographic studies throughout the sampled regions. These analyses on Pogonomyrmex harvester ants reveal a complex pattern of vicariance and dispersal that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid-adapted taxa in North America.Dissertation/ThesisM.S. Biology 201