Host-parasite coevolution

Questions and aims

We still know little about the molecular underpinnings of coevolution in natural populations: How many genes are involved, and are they identical across environments? What is the speed of coevolution, and does it vary across environments? What are the selective pressures acting on these genes? How does coevolution affect the evolution of other host life-history traits such as seed dormancy?

Plant-parasite interactions provide particularly suitable model systems for molecular ecology studies as there has been a substantial emphasis in recent years on dissecting the genetic and molecular architecture of host-parasite specificity (Jones and Dangl, Nature, 2006). Coevolutionary models suggest that reciprocal changes of allele frequencies over time at genes involved in host and parasite interactions can follow two simple scenarios (Woolhouse et al., Nature Genet., 2002; Holub, Nat. Rev. Genet., 2001): the ‘arms-race’ scenario, which is a series of recurrent selective sweeps, and the ‘trench warfare’ (or balancing selection) scenario (Stahl et al., Nature, 1999), which maintains alleles at intermediate frequencies due to frequency-dependent selection.
Using as a case study the gene-for-gene interactions (GFG) between host (plant or animal) resistance genes and parasite effectors, we have shown that a fundamental mathematical condition, direct frequency-dependence selection, is necessary for the occurrence of balancing selection and is promoted by various plant and parasite life-history traits and ecological characteristics (review in Brown and Tellier, Annu Rev Phytopathol, 2011 ): e.g. seed banks and perenniality (Tellier and Brown, Am Nat, 2009) or parasite polycyclicity (Tellier and Brown, Proc Roy Soc B, 2007; Tellier and Brown, Genetics, 2007). The occurrence of arms race or trench warfare dynamics thus depends on a few key coevolutionary parameters (ecological and genetic costs). Moreover, environmental variability also has a crucial influence on coevolution (the ‘Geographic Mosaic Theory of Coevolution’ Thompson, 2005), specifically in GFG interactions (Tellier and Brown, BMC Evol Biol, 2011; Laine and Tellier, Oikos, 2008). These theoretical developments lay the foundations for a quantitative understanding of the major ecological mechanisms driving the molecular evolution of host defence genes in natural populations

Recently, I have developed models to predict more accurately the genomic signatures of coevolution at host and parasite loci of interaction (Tellier et al. Evolution 2014).

We aim to test these theoretical models of coevolution using genomic data for multiple populations of hosts and parasites.



Current projects

1) Development of finite population models of coevolution to investigate the effect of genetic drift on the behaviour of the dynamical system (stability of the equilibrium). This work is conducted in collaboration with Wolfgang Stephan (LMU, Munich, Germany). This work is funded by the DFG Priority Program SPP1590.

2) Development of methods to study host-parasite coevolution using population genomic data. This work is funded the the DFG Priority Program SPP1819.

We have developed mathematical models of coevolution (Stephan and Tellier 2020) with eco-evo feedback (Živković et al. 2019) and ABC method to estimate parameters of coevolution (Märkle and Tellier 2020) and published recently a review on methods for coevolutionary genomics (Märkle et al. 2021). A summary of coevolution theory and genomics is found in our recent Tellier et al. (2021).



Funding DFG programs: SPP 1590 and SPP 1819

Pictures below from Brown and Tellier, Annu Rev Phytopathol, 2011.

Gene-for-gene cycles and equilibrium stability

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Polycyclicity and direct frequency-dependent selection

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