Pamminger T, Modlmeier A, Suette S, Pennings PS, Foitzik S. Raiders from the sky: slavemaker founding queens select for aggressive host colonies. Biology Letters [Internet]. 2012. Video 2012pammingerbiolettpreprint.pdf
Pamminger T, Leingaertner A, Achenbach A, Kleeberg I, Pennings PS, Foitzik S. Geographic distribution of the anti-parasite trait “slave rebellion”. Evolutionary Ecology. 2012. 2012pamminger_evol_ecol_preprint.pdf
Domingues VS, Poh Y-P, Peterson BK, Pennings PS, Jensen JD, Hoekstra HE. Evidence of adaptation from ancestral variation in young populations of beach mice. Evolution [Internet]. 2012. Website dominguesetalevolutioninpress.pdf
Pennings PS. Standing genetic variation and the evolution of drug resistance in HIV. PLoS Comp Biol [Internet]. 2012;8 (6) :e1002527. Video abstractAbstract

Drug resistance remains a major problem for the treatment of HIV. Resistance can occur due to mutations that were present before treatment starts or due to mutations that occur during treatment. The relative importance of these two sources is unknown. We study three different situations in which HIV drug resistance may evolve: starting triple-drug therapy, treatment with a single dose of nevirapine and interruption of treatment. For each of these three cases good data are available from literature, which allows us to estimate the probability that resistance evolves from standing genetic variation. Depending on the treatment we find probabilities of the evolution of drug resistance due to standing genetic variation between 0 and 39%. For patients who start triple-drug combination therapy, we find that drug resistance evolves from standing genetic variation in approximately 6% of the patients. We use a population-dynamic and population-genetic model to understand the observations and to estimate important evolutionary parameters. We find that both, the effective population size of the virus before treatment, and the fitness of the resistant mutant during treatment, are key-parameters that determine the probability that resistance evolves from standing genetic variation. Importantly, clinical data indicate that both of these parameters can be manipulated by the kind of treatment that is used.

Pamminger T, Scharf I, Pennings PS, Foitzik S. Increased host aggression as an induced defense against slave-making ants. Behavioral Ecology. 2011;22 (2) :255-260.Abstract
Slave-making ants reduce the fitness of surrounding host colonies through regular raids, causing the loss of brood and frequently queen and worker death. Consequently, hosts developed defenses against slave raids such as specific recognition and aggression toward social parasites, and indeed, we show that host ants react more aggressively toward slavemakers than toward nonparasitic competitors. Permanent behavioral defenses can be costly, and if social parasite impact varies in time and space, inducible defenses, which are only expressed after slavemaker detection, can be adaptive. We demonstrate for the first time an induced defense against slave-making ants: Cues from the slavemaker Protomognathus americanus caused an unspecific but long-lasting behavioral response in Temnothorax host ants. A 5-min within-nest encounter with a dead slavemaker raised the aggression level in T. longispinosus host colonies. Contrarily, encounters with nonparasitic competitors did not elicit aggressive responses toward non-nestmates. Increased aggression can be adaptive if a slavemaker encounter reliably indicates a forthcoming attack and if aggression increases postraid survival. Host aggression was elevated over 3 days, showing the ability of host ants to remember parasite encounters. The response disappeared after 2 weeks, possibly because by then the benefits of increased aggression counterbalance potential costs associated with it.
Pennings PS, Achenbach A, Foitzik S. Similar evolutionary potentials in an obligate ant parasite and its two host species. Journal of Evolutionary Biology. 2011;24 (4) :871–886.Abstract
The spatial structure of host–parasite coevolution is shaped by population structure and genetic diversity of the interacting species. We analysed these population genetic parameters in three related ant species: the parasitic slavemaking ant Protomognathus americanus and its two host species Temnothorax longispinosus and T. curvispinosus. We sampled throughout their range, genotyped ants on six to eight microsatellite loci and an MtDNA sequence and found high levels of genetic variation and strong population structure in all three species. Interestingly, the most abundant species and primary host, T. longispinosus, is characterized by less structure, but lower local genetic diversity. Generally, differences between the species were small, and we conclude that they have similar evolutionary potentials. The coevolutionary interaction between this social parasite and its hosts may therefore be less influenced by divergent evolutionary potentials, but rather by varying selection pressures. We employed different methods to quantify and compare genetic diversity and structure between species and genetic markers. We found that Jost D is well suited for these comparisons, as long as mutation rates between markers and species are similar. If this is not the case, for example, when using MtDNA and microsatellites to study sex-specific dispersal, model-based inference should be used instead of descriptive statistics (such as D or GST). Using coalescent-based methods, we indeed found that males disperse much more than females, but this sex bias in dispersal differed between species. The findings of the different approaches with regard to genetic diversity and structure were in good accordance with each other.
Goering LM, Hunt PK, Heighington C, Busick C, Pennings PS, Hermisson J, Kumar S, Gibson G. Association of orthodenticle with Natural Variation for Early Embryonic Patterning in Drosophila melanogaster. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution. 2009;312B (8) :841-854.Abstract
Although it is well established that cis-acting regulatory variation contributes to morphological evolution between species, few concrete examples of polymorphism affecting developmental patterning within species have been demonstrated. Early embryogenesis in Drosophila is initiated by a gradient of Bicoid morphogen activity that results in differential expression of multiple target genes. In a screen for genetic variation affecting this process, we surveyed 96 wild-type lines of Drosophila melanogaster for polymorphisms in binding sites within 16 Bicoid cis-regulatory response elements. One common polymorphism in the orthodenticle (otd) early head enhancer is associated with a complex series of indels/substitutions that define two distinct haplotypes. The middle region of this enhancer exhibits an unusual pattern of nucleotide diversity that does not easily fit into standard models of selection and demography. Population Gene Expression Maps, generated by extracting binary expression profiles from normalized embryo images, revealed a ventral reduction of otd transcript abundance in one of the haplotypes that was recapitulated in expression of transgenic constructs containing the two alleles. We thus demonstrate that even a process as robust as early developmental patterning is affected by standing genetic variation, intriguingly involving otd, whose morphogenetic function bicoid is thought to have displaced during dipteran evolution. J. Exp. Zool. (Mol. Dev. Evol.) 312B:841-854, 2009. (C) 2009 Wiley-Liss, Inc.
Foitzik S, Bauer S, Laurent S, Pennings PS. Genetic diversity, population structure and sex-biased dispersal in three co-evolving species. Journal of Evolutionary Biology. 2009;22 (12) :2470-2480.Abstract
Genetic diversity and spatial structure of populations are important for antagonistic coevolution. We investigated genetic variation and population structure of three closely related European ant species: the social parasite Harpagoxenus sublaevis and its two host species Leptothorax acervorum and Leptothorax muscorum. We sampled populations in 12 countries and analysed eight microsatellite loci and an mtDNA sequence. We found high levels of genetic variation in all three species, only slightly less variation in the host L. muscorum. Using a newly introduced measure of differentiation (Jost's D-est), we detected strong population structuring in all species and less male-biased dispersal than previously thought. We found no phylogeographic patterns that could give information on post-glacial colonization routes - northern populations are as variable as more southern populations. We conclude that conditions for Thompson's geographic mosaic of coevolution are ideal in this system: all three species show ample genetic variation and strong population structure.
Pennings PS, Kopp M, Meszena G, Dieckmann U, Hermisson J. An analytically tractable model for competitive speciation. American Naturalist. 2008;171 (1) :E44-E71.Abstract
Several recent models have shown that frequency-dependent disruptive selection created by intraspecific competition can lead to the evolution of assortative mating and, thus, to competitive sympatric speciation. However, since most of these results rely on limited numerical analyses, their generality has been debated. Here, we consider one of the standard models (the so-called Roughgarden model) with a simplified genetics where the selected trait is determined by a single diallelic locus. This model is sufficiently complex to maintain key properties of the general multilocus case but simple enough to allow for comprehensive analytical treatment by means of invasion fitness arguments. Depending on (1) the strength and (2) the shape of stabilizing selection, (3) the strength and (4) the shape of pairwise competition, (5) the shape of the mating function, and (6) whether assortative mating leads to sexual selection, we find five different evolutionary regimes. In one of these regimes, complete reproductive isolation can evolve through arbitrarily small steps in the strength of assortative mating. Our approach provides a mechanistic understanding of several phenomena that have been found in previous models. The results demonstrate how even in a simple model, the evolutionary outcome depends in a complex way on ecological and genetic parameters.
Sicard D, Pennings PS, Grandclement C, Acosta J, Kaltz O, Shykoff JA. Specialization and local adaptation of a fungal parasite on two host plant species as revealed by two fitness traits. Evolution. 2007;61 (1) :27-41.Abstract
We investigate the geographic pattern of adaptation of a fungal parasite, Colletotrichum lindemuthianum, on two host species, Phaseolus vulgaris and P coccineus for two parasite fitness traits: infectivity (ability to attack a host individual) and aggressivity (degree of sporulation and leaf surface damage). Using a cross-inoculation experiment, we show specialization of the fungus on its host species of origin for both traits even when fungi, which originated from hosts growing in sympatry, were tested on sympatric host populations. Within the two host species, we compared infectivity and aggressivity on local versus allopatric plant-fungus combinations. We found evidence for local adaptation for the two traits on P vulgaris but not on P coccineus. There was no significant correlation between the degrees of local adaptation for infectivity and aggressivity, indicating that the genetic basis and the effect of selection may differ between these two traits. For the two fitness traits, a positive correlation between the degree of specialization and the degree of local adaptation was found, suggesting that specialization can be reinforced by local adaptation.
Pennings PS, Hermisson J. Soft sweeps III: The signature of positive selection from recurrent mutation. Plos Genetics. 2006;2 (12) :1998-2012.Abstract
Polymorphism data can be used to identify loci at which a beneficial allele has recently gone to fixation, given that an accurate description of the signature of selection is available. In the classical model that is used, a favored allele derives from a single mutational origin. This ignores the fact that beneficial alleles can enter a population recurrently by mutation during the selective phase. In this study, we present a combination of analytical and simulation results to demonstrate the effect of adaptation from recurrent mutation on summary statistics for polymorphism data from a linked neutral locus. We also analyze the power of standard neutrality tests based on the frequency spectrum or on linkage disequilibrium (LD) under this scenario. For recurrent beneficial mutation at biologically realistic rates, we find substantial deviations from the classical pattern of a selective sweep from a single new mutation. Deviations from neutrality in the level of polymorphism and in the frequency spectrum are much less pronounced than in the classical sweep pattern. In contrast, for levels of LD, the signature is even stronger if recurrent beneficial mutation plays a role. We suggest a variant of existing LD tests that increases their power to detect this signature.
Pennings PS, Hermisson J. Soft sweeps II-molecular population genetics of adaptation from recurrent mutation or migration. Molecular Biology and Evolution. 2006;23 (5) :1076-1084.Abstract
In the classical model of molecular adaptation, a favored allele derives from a single mutational origin. This ignores that beneficial alleles can enter a population recurrently, either by mutation or migration, during the selective phase. In this case, descendants of several of these independent origins may contribute to the fixation. As a consequence, all ancestral haplotypes that are linked to any of these copies will be retained in the population, affecting the pattern of a selective sweep on linked neutral variation. In this study, we use analytical calculations based on coalescent theory and computer simulations to analyze molecular adaptation from recurrent mutation or migration. Under the assumption of complete linkage, we derive a robust analytical approximation for the number of ancestral haplotypes and their distribution in a sample from the population. We find that so-called "soft sweeps," where multiple ancestral haplotypes appear in a sample, are likely for biologically realistic values of mutation or migration rates.
Hermisson J, Pennings PS. Soft sweeps: Molecular population genetics of adaptation from standing genetic variation. Genetics. 2005;169 (4) :2335-2352.Abstract
A population can adapt to a rapid environmental change or habitat expansion in two ways. It may adapt either through new beneficial mutations that subsequently sweep through the population or by using alleles from the standing genetic variation. We rise diffusion theory to calculate the probabilities for selective adaptations and find a large increase in the fixation probability for weak substitutions, if alleles originate from the standing genetic variation. We then determine the parameter regions where each scenario-standing variation vs. new mutations-is more likely. Adaptations front the standing genetic variation are favored if either the selective advantage is weak or the selection coefficient and the mutation rate are both high. Finally, we analyze the probability of "soft sweeps," where multiple copies of the selected allele contribute to a substitution, and discuss the consequences for the footprint of selection on linked neutral variation. We find that soft sweeps with weaker selective footprints are likely tinder both scenarios if the mutation rate and/or the selection coefficient is high.
Collin CL, Pennings PS, Rueffler C, Widmer A, Shykoff JA. Natural enemies and sex: how seed predators and pathogens contribute to sex-differential reproductive success in a gynodioecious plant. Oecologia. 2002;131 (1) :94-102.Abstract
In insect-pollinated plants flowers must balance the benefits of attracting pollinators with the cost of attracting natural enemies, when these respond to floral traits. This dilemma can have important evolutionary consequences for mating-system evolution and polymorphisms for floral traits. We investigate the benefits and risks associated with flower size and sex morph variation in Dianthus sylvestris, a gynodioecious species with pistillate flowers that are much smaller than perfect flowers. We found that this species is mainly pollinated by nocturnal pollinators, probably moths of the genus Hadena, that also oviposit in flowers and whose caterpillars feed on developing fruits and seeds. Hadena preferred larger flowers as oviposition sites, and flowers in which Hadena had deposited eggs bore more pollen on their stigmas, suggesting that Hadena is indeed the principle pollinator, or that pollinators and these seed predators employ the same choice criteria for flowers. Globally, perfect flowers suffered more predation by seed predators than did pistillate flowers, suggesting that seed predators play an important role in reproductive system dynamics in this species. On the other hand, female flowers were more likely to be contaminated with spores of another natural enemy, the pathogenic fungus Microbotryum violaceum, that are transmitted by pollinating insects. This complex interplay between two natural enemies, one of which, Hadena, is also a pollinator and vector of fungal spores, may contribute to the maintenance of the polymorphic reproductive system of the host plant.
Rigaud T, Pennings PS, Juchault P. Wolbachia bacteria effects after experimental interspecific transfers in terrestrial isopods. Journal of Invertebrate Pathology. 2001;77 (4) :251-257.Abstract
Wolbachia bacteria are intracellular parasites, vertically transmitted from mothers to offspring through the cytoplasm of the eggs. They manipulate the reproduction of their hosts to increase in frequency in host populations. In terrestrial isopods for example, Wolbachia are responsible for the full feminization of putative males, therefore increasing the proportion of females, the sex by which they are transmitted. Vertical transmission, however, is not the only means for Wolbachia propagation. Infectious (i.e., horizontal) transmission between different host species or taxa is required to explain the fact that the phylogeny of Wolbachia does not parallel that of their hosts. The aim of this study was to investigate, by experimental transinfections, whether Wolbachia strains could be successfully transferred to a different, previously uninfected isopod host. While Wolbachia survived in all the studied recipient species, vertical transmission was efficient only in cases where donor and recipient species were closely related. Even in this case, Wolbachia strains did not always keep their ability to entirely feminize their host, a deficiency that can be link to a low bacterial density in the host tissues, In addition, Wolbachia infection was associated with a decrease in host fertility, except when the bacterial strain came from the same host population as the recipient animals, This suggest that Wolbachia could be adapted to local host populations. It therefore seems that isopod Wolbachia are highly adapted to their host and can hardly infect another species of hosts. The successful infection of a given Wolbachia strain into a new isopod host species therefore probably requires a strong selection on bacterial variants. (C) 2001 Academic Press.