Volume 119, Issue 4, August 2016, Pages 330–338

SI: Host-Parasite Coevolution

Edited By Joachim Kurtz, Hinrich Schulenburg and Thorsten B.H. Reusch

Review

Host–parasite coevolution: why changing population size matters

  • a Department of Evolutionary Ecology and Genetics, Christian-Albrechts-University of Kiel, 24098, Kiel, Germany
  • b New Zealand Institute for Advanced Study, Massey University, Private Bag 102904, Auckland 0745, New Zealand
  • c Department of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, August-Thienemann-Straße 2, 24306 Plön, Germany

Highlights

Host–parasite interactions often affect the population dynamics of the two antagonists.

Parasites in particular often undergo extreme bottlenecks during their life cycle.

Such demographic changes can affect genetic variation and selection–drift interplay.

Demographic changes can thus have a central influence on the dynamics of coevolution.


Abstract

Host–parasite coevolution is widely assumed to have a major influence on biological evolution, especially as these interactions impose high selective pressure on the reciprocally interacting antagonists. The exact nature of the underlying dynamics is yet under debate and may be determined by recurrent selective sweeps (i.e., arms race dynamics), negative frequency-dependent selection (i.e., Red Queen dynamics), or a combination thereof. These interactions are often associated with reciprocally induced changes in population size, which, in turn, should have a strong impact on co-adaptation processes, yet are neglected in most current work on the topic. Here, we discuss potential consequences of temporal variations in population size on host–parasite coevolution. The limited empirical data available and the current theoretical literature in this field highlight that the consideration of such interaction-dependent population size changes is likely key for the full understanding of the coevolutionary dynamics, and, thus, a more realistic view on the complex nature of species interactions.

Keywords

  • Host–parasite coevolution;
  • Population size dynamics;
  • Negative frequency-dependent selection;
  • Recurrent selective sweeps;
  • Genetic drift;
  • Population bottlenecks

1. Introduction

Over the past decades host–parasite coevolution has received particular scientific interest because it is associated with very high selective constraints, resulting in fast and complex evolutionary dynamics that affect a large variety of trait functions (Woolhouse et al., 2002). On the one hand, parasite-induced reduction in host fitness enhances selection for host resistance mechanisms. On the other hand, novel host defences increase selection on the parasite. Genetic variants (alleles) conferring an advantage in the antagonistic interaction can rapidly spread through the population and go to fixation (Buckling and Rainey, 2002). Ultimately, this can lead to so-called recurrent selective sweeps (RSS) or arms race dynamics, consisting of a series of fixation events occurring sequentially or even in parallel in host and parasite (Fig.  1A). Alternatively, an allele may only provide an advantage when rare and would be disfavoured as it increases in frequency in the population (e.g., because parasites have a resource advantage when targeting the common host genotypes). Allele frequency changes in the host population would then cause a corresponding allele frequency change in the parasite population and vice versa, leading to continuous negative frequency-dependent allele oscillations (i.e, negative frequency-dependent selection, NFDS), which are often referred to as Red Queen dynamics (Decaestecker et al., 2007). NFDS can favour the coexistence of several alleles over long time periods (Fig.  1B).

Allele frequency dynamics during host–parasite coevolution. (A) Recurrent ...
Fig. 1. 

Allele frequency dynamics during host–parasite coevolution. (A) Recurrent selective sweeps (RSS) and (B) negative frequency-dependent selection (NFDS).

Both types of selection dynamics, RSS and NFDS, are supported by experimental studies (Buckling and Rainey, 2002, Decaestecker et al., 2007, Betts et al., 2014 and Gómez et al., 2015), but their exact role in natural host–parasite interactions is not fully understood. As highlighted in different articles of the current issue and also additional studies, various factors are likely to shape the coevolutionary dynamics. These include, for example, genetic diversity (Lively and Apanius, 1995), the genetic system of the interaction (Agrawal and Lively, 2002), different aspects of life history (Barrett et al., 2008; see also an article in the current issue by Strauss et al., 2016), epidemiological characteristics (Tellier and Brown, 2007; see also an article in the current issue by González-Tortuero et al., 2016), metapopulation structure (Gandon and Michalakis, 2002 and Thrall and Burdon, 2002), fluctuating environmental changes (Wolinska and King, 2009), phenotypic plasticity, epigenetics, and tolerance (reviewed in the current issue by Kutzer and Armitage, 2016, Milutinović et al., 2016 and Vilcinskas, 2016), social interactions within the host taxon (reviewed in the current issue by Kurze et al., 2016; Joop and Vilcinskas, 2016), and the presence of multiple parasites (reviewed in the current issue by Bose et al., 2016). Paradoxically, one important outcome of the host–parasite interaction, namely population size changes, is usually not taken into account. In fact, the influence of population size is excluded from many theoretical models of coevolution (for some exceptions see May and Anderson, 1983, Frank, 1991, Frank, 1993, Gandon et al., 1996, Quigley et al., 2012, Gokhale et al., 2013, Ashby and Gupta, 2014 and Song et al., 2015) and kept constant, where possible, in experimental systems (Bérénos et al., 2009, Greeff and Schmid-Hempel, 2010 and Schulte et al., 2010). This is surprising, because host–parasite interactions are often associated with dramatic changes in population size (Section 2), and such changes are usually an integral part of epidemiological processes (e.g., transmission bottleneck, Section 3). Therefore, it is pivotal to elucidate their role in reciprocal adaptations between host and parasite.

In the present paper, we review the evidence for temporal changes in population size induced by host–parasite interactions and discuss their consequences for coevolution (Section 4). As population size has a central influence on the process of adaptation and as enormous demographic changes can occur during host–parasite interactions, further empirical and theoretical studies are required to systematically assess the role of such temporal population size variations in shaping coevolutionary dynamics (Section 5).