The evolution of parasite genomes and the origins of parasitism

From a human perspective it seems intuitive to view life as essentially free-living, and parasites as specialized derivatives. Certainly, this is the impression given by biology teaching or the balance of research effort. In fact, it is just conceivable that parasites are more numerous than non-parasites (Dobson et al. 2008), and while this may be difficult to prove, they are clearly abundant and ubiquitous throughout evolutionary history (Conway Morris, 1981). Today, we appreciate the great importance parasites have for the ecology, behaviour and evolution of free-living organisms, but also for biodiversity and ecosystem function (Lafferty et al. 2006; Kuris et al. 2008; Dunne et al. 2013). As moderators of trophic dynamics and competition between free-living species, parasites have been called ‘ecosystem engineers’ (Hatcher et al. 2012) and as vital components of all ecosystems the evolutionary origins of parasites are a core issue in evolutionary biology, although it has not always been so. In April 2013, parasitologists working on various parasites and with diverse approaches met at the Wellcome Trust Conference Centre in Hinxton (UK) for a meeting entitled ‘The evolution of parasite genomes and the origins of parasitism’. The purpose of the meeting was to promote consensus on the impact of genomics on the evolution of parasitism and to identify any themes in genome evolution that cut across taxonomic boundaries. Most research communities are now approaching a point where genome sequences exist for multiple species of their chosen parasite. Therefore, the question of origins and diversification are being posed in many quarters. In principle, the wealth of comparative genomic data provides an opportunity to test long-standing hypotheses of genome reduction, adaptation, the evolution of complexity, and host–parasite co-evolution with unprecedented accuracy and clarity. This special issue contains ten review articles developing the discussions that took place. From the 19th century birth of evolutionary biology until well into the 20th century, parasites were seen as biologically degenerate, ecologically marginal and evolutionarily anomalous. The first generation of evolutionary thinkers retained a belief that evolution was progressive and tending towards perfection. Cope’s 1896 Law that evolution proceeds from unspecialized to specialized forms left parasites estranged; they had specialized in regression. Whether this was a lingering sense of orthogenesis, the afterglow of a Scala Naturae, or an ingrained anthropocentricity, evolutionary biologists struggled to see parasites, apparently an insult to evolutionary progress, as fully fledged organisms, and considered parasitic adaptations less authentic than those of nonparasites. Vickerman (2009) describes how this atmosphere contributed to the insularity of parasitology and its poor relationship with the study of evolution. The comment by Konrad Lorenz, as late as 1973, that ‘If one judges the adapted forms of the parasites according to the amounts of retrogressed information, one finds a loss of information that coincides with and completely confirms the low estimation we have of them and how we feel about them’ is worth repeating because it encapsulates the engrained view that becoming a parasite is mostly about inexorable degradation. Today, any concept of progress in evolution is based on fitness metrics that define parasites as well as any organism. While we have discarded the notions of directionality and chauvinism that prejudiced our analysis of parasitism, it casts a pall over parasite evolution and affects the questions we tend to ask. The arrival of molecular phylogenetics made it possible to consider the origin and diversification of parasites explicitly and with sufficient power. Parasites are now a subject for evolutionary biologists, who consider their roles in the origins of sex and in speciation, while evolution is a subject * Corresponding author: Department of Infection Biology, University of Liverpool, Liverpool Science Park, Ic2 Building, 146 Brownlow Hill, Liverpool, Merseyside, UK. E-mail: a.p.jackson@liv.ac.uk S1 SPECIAL ISSUE ARTICLE