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From hybrids to hermaphrodites in population genetics


A report on the 46th annual PopGroup conference, Glasgow, UK, December 18-21,2012.

Shortly before Christmas 2012, the 46th PopGroup (Population Genetics Group) meeting washeld at Glasgow University, UK. Over 180 scientists attended from 19 differentcountries, with speakers from diverse research areas and ranging from PhD students toretired professors. Some talks dealt with the conservation of exotic species on remoteislands, while others took a more theoretical approach. Almost all made use of, oranticipated, the volume and ever-reducing cost of data from next-generation sequencing,which is opening up access to research topics and study organisms that were previouslyoff limits. Here, we report on some of the main themes of the conference, and thedirections in which next-generation sequencing technology is taking us.

Hybridization in non-model organisms

In the opening plenary talk, Michael Arnold (University of Georgia, Athens, USA)recounted how his long-term population genetic research on hybrids of the Louisiana Irishas unfolded. An apparently disastrous flood changed the direction of one of Arnold'slarge-scale field experiments, providing evidence that the proportion of introgressedgenes from one parental species dictated how well individuals survived flooding. Arecurring theme of the conference, particularly in the study of genetic introgression,was that dissection of such effects in non-model organisms in their natural environmentwas most effective through the combination of new sequencing technologies with fieldsurveys, experimentation and hard-won biological insights.

This combination was exemplified by the work on hybridization between two subspecies ofthe grasshopper Chorthippus parallelus presented by James Hutchison (Universityof Sheffield, UK). Whereas laboratory crosses between the two taxa produce sterilemales, the offspring produced in a narrow hybrid zone in the Pyrenees mountain rangeseem to be fully fertile. This result could be explained by thousands of years ofselection, which might, for example, drive key sterility alleles out of the zone. Buthow could the key loci be identified from the many differences between the taxa acrossthe whole genome? Hutchison evaluated candidate loci from expression data by analyzingallele frequency differences across the zone. This strategy exploits the long history ofcrossing, backcrossing, gene flow and selection producing the frequency differences.

In the case of trees, a long temporal perspective is provided by the living individualsthemselves. Kirsten Wolff (Newcastle University, UK) presented preliminary results onhybridization in lime trees. Ancestors, perhaps thousands of years old, live alongsidetheir descendants, making them living fossil records and facilitating direct geneticcomparisons over these extraordinary timescales. On the other hand, the existence ofoverlapping generations with their genetic contribution to new offspring presents ananalytical challenge in the form of incomplete lineage sorting.

Theoretical surprises

The wealth of data provided by next-generation sequencing methods brings with it thestatistical power to detect evolutionary change at a high resolution. Theoretical modelsplay an important role here, separating evolutionary signal from noise and providingtentative explanations for differences throughout the genome. This year's theoreticaltalks put forward some novel and unexpected predictions that in some cases went so faras to defy the conventional wisdom. Daniel Weissman (Institute of Science andTechnology, Klosterneuberg, Austria) gave a prize-winning talk about thecounterintuitive effects of selective sweeps. Using both analytical theory andsimulation, Weissman demonstrated that the random origin of advantageous mutations in atwo-dimensional bounded population systematically distorts the pattern of ancestry.These mutations seed selective sweeps spreading out to the species' margins, such thatthe ancestry of the adjacent part of the genome will trace back toward the center of thespecies' range, resulting in a pattern of neutral variation that could be easilymistaken for a range expansion.

In the case of genuine range expansions, Jens Nullmeier (Max Planck Institute forDynamics and Self-Organization, Göttingen, Germany) argued for a clear distinctionbetween phenotype-limited range expansions and those in which the population is limitedby a slowly moving boundary. Nullmeier developed a coalescent model, and concluded thatthe different types of range expansions leave different genetic footprints, which canpotentially be used to infer past population histories.

Another prize-winning talk exploited genome-wide data to explore some challengesinherent in estimating species divergence times from very large numbers of genes.Richard Nichols (Queen Mary University of London, UK) analyzed a dataset of thousands ofgenes across vertebrate genomes, and discovered that estimates of the time to the lastcommon ancestor of humans and chimpanzees vary greatly between human chromosomes. Yetmost discrepancies could be resolved when certain multi-gene families were removed fromthe analysis, suggesting that gene conversion might be at play in driving thisphenomenon. Following up with a theoretical model, Nichols demonstrated that geneconversion accelerates the rate at which species differentiate, particularly in theperiod immediately after speciation. If ignored, this effect could grossly distortestimates of divergence time or effective population size for surrounding parts of thegenome.

Genome-wide data can also be used to characterize allele frequencies at a large numberof loci within the same species, as demonstrated by Brian Charlesworth (University ofEdinburgh, UK), who presented work exploring the effects of mutational bias onstabilizing selection. Most standard evolutionary models predict that selection is moreeffective in large populations than in small populations as a result of weaker geneticdrift. However, by introducing mutational bias into a model of stabilizing selection,the scaled intensity of selection is nearly independent of effective population sizeover a wide range of parameter space; if this model holds true, then it may beimpossible to distinguish between stabilizing and directional selection from allelefrequency data alone.

A role for sex?

Another challenge of moving from the laboratory into the natural world is thatpresent-day biology will differ from that which shaped the evolution of the genome. Evenattributes as fundamental as breeding systems are labile: Deborah Charlesworth(University of Edinburgh, UK) presented work on the breakdown of dioecy (separate sexes)to gynodioecy (females and hermaphrodites) in angiosperms. A dioecious populationevolves to the gynodioecious form of sexuality when males become hermaphrodites byacquiring some female attributes. The study modeled the common gynodioecious situationand found that the frequency of females can be higher than hermaphrodites if the femalesoutnumber the males in the ancestral dioecious population.

Sonia Consuegra (Aberystwyth University, UK) explored the reasons why the fishKryptolebias marmoratus might maintain some sexuality in an androdioeciouspopulation with many selfing hermaphrodite lineages. Consuegra's group found that, givena choice, males exhibited a mating preference for the more genetically different mate,although, intriguingly, the hermaphrodites did not. The observation of higher parasitelevels in individuals derived from self-fertilization may explain the continuedexistence of males in this system.

Heidi Aisala (University of Oulu, Finland) examined the balance of cloning and sexualreproduction in fish parasites. Parasites from the genus Gyrodactylus arepredominantly host-specific, but with occasional sexual reproduction they can gain thecapacity to switch host species. Thereafter they can continue their clonal reproduction,needing only one individual to start the new population. This strategy has proved highlysuccessful, to the extent that Gyrodactylus host-switching is becoming a majoreconomic and ecological problem. The movement of infected individuals by fish farmershas allowed the parasite to invade local waterways and jump to new fish species.

Opening up the scientific process

Probably one of the most controversial talks at the conference was the final plenarytalk, entitled 'Why I blog instead of writing papers', by Roderic Page (University ofGlasgow, UK). A few years ago, Page shifted the balance of his publication towardblogging and away from writing academic papers. In a spirited debate, the audienceraised concerns that this method of communication is more self-centered thanconventional publishing. However, Page insisted that the use of blogging encouragesfeedback and ensures that science is a two-way discussion, as it should be. Page lookedforward to a time when DOIs (digital object identifiers, such as those used for onlinearticles in academic journals) are made available for blog posts, thereby making themmore readily citable. He argued that these hoped for citable blog posts will be thefuture mode of communicating science. There are clearly still open questions as to howthis scenario would work with regard to peer review and ownership of results, but Pagenevertheless predicts that the worlds of blogging and academic publishing will begin tomerge.


The technological advances of the last few years are changing the way we do andcommunicate science. Next-generation sequencing technologies allow for large scale andhigh-resolution analyses of individuals and populations, revealing surprising patternsthat feed directly back into the theoretical models. The way in which we communicateresults is also being altered by blogging and other social media, and is forcing us torethink the way we interact with the scientific community, as well as with thepopulation at large. All in all, this is an exciting time in population genetics.



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We thank the conference organizers, especially Barbara Mable, the Marie-Curie InitialTraining Network INTERCROSSING for funding the authors, and Richard Nichols forcomments.

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Correspondence to Robert Verity.

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The authors declare that they have no competing interests.

Robert Verity, Jeannine Marquardt, Andrea Hatlen and Jasmin Zohren contributed equally to this work.

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Verity, R., Marquardt, J., Hatlen, A. et al. From hybrids to hermaphrodites in population genetics. Genome Biol 14, 301 (2013).

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