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Parasites Opt for the Best of Both Worlds INSIGHT REPRODUCTION Parasites opt for the best of both worlds The fungal parasite Podosphaera plantaginis employs both sexual and asexual reproduction to increase its chances of infecting the plant Plantago lanceolata. ELLEN DECAESTECKER AND LORE BULTEEL plantaginis, which commonly infects the plant Related research article Laine A-L, Barre`s species Plantago lanceolata, commonly known B, Numminen E, Siren JP. 2019. Variable as ribwort plantain (Figure 1). These fungi asex- opportunities for outcrossing result in hot- ually reproduce by producing infective spores spots of novel genetic variation in a patho- throughout their life-cycle. When the host’s gen metapopulation. eLife 8:e47091. DOI: growing season comes to an end P. plantaginis 10.7554/eLife.47091 produce resting spores that can survive the win- ter. These spores can either be produced via mating, or via an asexual process known as hap- loid selfing that involves spores from the same organism ’mating’ with each other ost populations of animals produce (Tollenaere and Laine, 2013; Figure 1). Repro- genetically different offspring via sex- ducing sexually, however, comes at a much M ual reproduction. A small minority of greater cost, bringing into question why patho- animals, however, use asexual reproduction to gens continue to maintain this reproductive produce offspring that are genetically identical strategy. to the parent. Both strategies have their advan- One possible explanation comes from an evo- tages and weaknesses, and some animals actu- lutionary theory known as the Red Queen ally alternate between sexual and asexual hypothesis. Hosts and parasite species con- reproduction (Decaestecker et al., 2009). stantly evolve together in order to outcompete Most parasites reproduce asexually, but they one another: hosts co-evolve an increased resis- can switch to sexual reproduction to encourage tance, whilst parasites increase their ability to diversity and to remain infectious. Certain spe- infect. The Red Queen hypothesis proposes that cies of parasites can even sexually reproduce hosts with a co-evolving parasite are more likely with other species, via a process called hybrid- to reproduce sexually to increase genetic varia- ization. For example, some schistosome flat- tion in their offspring so they have a greater worms can infect a wider range of hosts, as a chance of evading infection. Parasites can then result of a bovine-infecting species mating with evolve quickly and continuously in response to Copyright Decaestecker and Bulteel. This article is distributed a human-infecting species (Huyse et al., 2009). the ongoing evolution of the host’s defenses. under the terms of the Creative This demonstrates how variation caused by This host-parasite arms race therefore offers an Commons Attribution License, which hybridization can increase the spread of a evolutionary advantage by helping maintain permits unrestricted use and disease. genetic variation in the population redistribution provided that the original author and source are Another parasite that reproduces both sexu- (Koskella and Lively, 2009; Decaestecker and credited. ally and asexually is the fungus Podosphaera King, 2019). Decaestecker and Bulteel. eLife 2019;8:e49615. DOI: https://doi.org/10.7554/eLife.49615 1 of 3 Insight Reproduction Parasites opt for the best of both worlds Figure 1. A simplified life cycle of the fungus P. plantaginis. The fungus P. plantaginis can reproduce both asexually (left) or sexually (right). Throughout the growing season P. plantaginis infects its host by asexually reproducing genetically identical clonal spores (represented by a dashed line). As the growing season of the host plant comes to an end, P. plantaginis produces a fruiting body known as chasmothecia, which contains resting spores that can survive the winter: these can either be reproduced asexually via process known as haploid selfing (left) or sexually via mating (right). When the next growing season starts, parasites can re-emerge from these resting spores and infect the host. Image credit: Lore Bulteel (CC BY 4.0). The time lag in co-evolution between these P. plantaginis with an increased number of co- two organisms largely depends on the evolution- infections were also found to have a larger num- ary potential (ability to genetically adapt in ber of new genotypes, suggesting that there are response to environmental pressures) of the par- localized hotspots of genetic diversity. asite (Gandon et al., 2008). However, much of Further work showed that these populations the evidence supporting the Red Queen hypoth- with a higher prevalence of co-infections (and esis has come from host populations, and the thus sexual reproduction) were also more likely evolutionary and ecological benefit of sexual to survive winter and initiate an infection the fol- reproduction in parasites has scarcely been lowing season. This higher success indicates that described. Now in eLife, Jukka P Sire´n of Aalto these newly generated genotypes can start pop- University and co-workers at the University of ulations that are better equipped at infecting Helsinki, University of Zurich and Universite´ Lyon the host plant. When the growing season starts, – including Anna-Liisa Laine as first author – this in turn could have an effect on the host pop- report evidence of sexual reproduction being ulation, and cause them to adapt a higher maintained in subpopulations of the fungal para- resistance. site P. plantaginis (Laine et al., 2019). Sub-populations of hosts and parasites will Laine et al. tracked the life-cycle of P. planta- co-evolve at different rates depending on their ginis subpopulations in the A˚ land Islands of Fin- surrounding environment: for example, in one land over four consecutive years. Analyzing the location the parasite may be ahead in the evolu- DNA sequences of every P. plantaginis specimen tionary arms race, while in another the host is revealed a number of new genotypes were winning. These differences in evolutionary rate being produced each year, suggesting that sex- are then reflected spatially, creating localized ual reproduction is common within this fungal pockets of emerging new genotypes (Thomp- species. For sexual reproduction to occur at son, 2005). By increasing genetic diversities in least two genotypically different parasites need these areas, parasites can ‘hedge their evolu- to infect the same host so they can be close tionary bets’ and deliver rare genotypes, which enough to exchange genetic material. Laine have lower fitness but could potentially thrive et al. showed the number of co-infected speci- under certain stressful environmental conditions mens was spatially varied across the population. (Starrfelt and Kokko, 2012). It would therefore Decaestecker and Bulteel. eLife 2019;8:e49615. DOI: https://doi.org/10.7554/eLife.49615 2 of 3 Insight Reproduction Parasites opt for the best of both worlds be interesting to explore how changes in selec- Biology of Parthenogenesis. Springer. p. 295–316. tion pressures between P. plantaginis and its DOI: https://doi.org/10.1007/978-90-481-2770-2_15 host effects the number of resting spores that Decaestecker E, King K. 2019. Red Queen Dynamics. In: Fath B (Ed). Encyclopedia of Ecology. 3 2nd are sexually produced. This could be achieved Edition. Elsevier. p. 185–192. by setting up a bank of P. plantaginis resting Gaba S, Ebert D. 2009. Time-shift experiments as a spores, and tracking their infections throughout tool to study antagonistic coevolution. Trends in the years to see how they relate to evolutionary Ecology & Evolution 24:226–232. DOI: https://doi.org/ 10.1016/j.tree.2008.11.005, PMID: 19201504 changes (Gaba and Ebert, 2009). Gandon S, Buckling A, Decaestecker E, Day T. 2008. Future challenges involve seeing if the results Host-parasite coevolution and patterns of adaptation obtained from this study can be reproduced by across time and space. Journal of Evolutionary Biology laboratory experiments, and untangling the pos- 21:1861–1866. DOI: https://doi.org/10.1111/j.1420- sible selective pressures and benefits of sexual 9101.2008.01598.x, PMID: 18717749 reproduction in parasites. It is also possible that Huyse T, Webster BL, Geldof S, Stothard JR, Diaw OT, Polman K, Rollinson D. 2009. Bidirectional sexually generated genetic changes in parasites introgressive hybridization between a cattle and could influence important ecological processes: human schistosome species. PLOS Pathogens 5: for example, genetic variation in parasites could e1000571. DOI: https://doi.org/10.1371/journal.ppat. make a change to the host’s shape, which then 1000571, PMID: 19730700 propagates throughout the population and dis- Koskella B, Lively CM. 2009. Evidence for negative frequency-dependent selection during experimental rupts the whole ecosystem. These changes in coevolution of a freshwater snail and a sterilizing the ecosystem could then fuel evolutionary trematode. Evolution 63:2213–2221. DOI: https://doi. changes in the parasite, resulting in a full feed- org/10.1111/j.1558-5646.2009.00711.x back loop of eco-coevolutionary interactions. Laine AL, Barre`s B, Numminen E, Siren JP. 2019. Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen Ellen Decaestecker is in the Department of Biology, metapopulation. eLife 8:e47091. DOI: https://doi.org/ Katholieke Universiteit Leuven Kulak, Kortrijk, Belgium 10.7554/eLife.47091, PMID: 31210640 Starrfelt J, Kokko H. 2012. Bet-hedging: A triple [email protected] trade-off
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