Volume 119, Issue 4, August 2016, Pages 375–383

SI: Host-Parasite Coevolution

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

Review

Effects of environmental variation on host–parasite interaction in three-spined sticklebacks (Gasterosteus aculeatus)

  • a Institute for Evolution and Biodiversity, Animal Evolutionary Ecology, University of Münster, Hüfferstrasse 1, D-48149 Münster, Germany
  • b Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, D-24306 Plön, Germany

Highlights

Sticklebacks adapt to the locally abundant parasite fauna.

High parasite infection pressure leads to the evolution of higher host resistance.

Parasites evolve higher virulence in resistant stickleback populations.

Temperature variation modulates host immunity and parasite virulence.

Rising temperature presumably results in higher parasite life cycle completion rates.


Abstract

Recent research provides accumulating evidence that the evolutionary dynamics of host–parasite adaptations strongly depend on environmental variation. In this context, the three-spined stickleback (Gasterosteus aculeatus) has become an important research model since it is distributed all over the northern hemisphere and lives in very different habitat types, ranging from marine to freshwater, were it is exposed to a huge diversity of parasites. While a majority of studies start from explorations of sticklebacks in the wild, only relatively few investigations have continued under laboratory conditions. Accordingly, it has often been described that sticklebacks differ in parasite burden between habitats, but the underlying co-evolutionary trajectories are often not well understood. With the present review, we give an overview of the most striking examples of stickleback–parasite–environment interactions discovered in the wild and discuss two model parasites which have received some attention in laboratory studies: the eye fluke Diplostomum pseudospathacaeum, for which host fish show habitat-specific levels of resistance, and the tapeworm Schistocephalus solidus, which manipulates immunity and behavior of its stickleback host to its advantage. Finally, we will concentrate on an important environmental variable, namely temperature, which has prominent effects on the activity of the immune system of ectothermic hosts and on parasite growth rates.

Keywords

  • Gasterosteus aculeatus;
  • Diplostomum pseudospathaceum;
  • Schistocephalus solidus;
  • Local adaptation;
  • Host–parasite interaction

1. Introduction

Recent research provides accumulating evidence that host–parasite interactions are strongly influenced by environmental variation (Lafferty, 1997, Lafferty and Kuris, 1999, Lazzaro and Little, 2009, Wolinska and King, 2009 and Schmid-Hempel, 2011). Consequently, wild host populations differ across habitat types in the diversity and intensity of parasite infections. Investigation of such natural diversity allows to elucidate the role of environmental effects for host–parasite interaction and coevolution (Eizaguirre et al., 2012a and Lenz et al., 2013).

In this context, the three-spined stickleback (Gasterosteus aculeatus) is a perfectly suited model organism, which has been extensively used in evolutionary ecology research ( Barber, 2013) as it is widely distributed across different habitat types and is a host to a variety of parasites. With the present review we aim to give an overview of the current knowledge of environmental influences on three-spined sticklebacks and their parasites. We will first look at phenomena of local host–parasite adaptation and thereafter discuss potential effects of temperature as an important environmental factor.

1.1. The three-spined stickleback model

When marine sticklebacks re-colonized rivers and lakes in coastal areas of the northern hemisphere after the last glaciation about 12,000 years ago (McPhail, 2007), they had to adapt to various new environmental conditions. In contrast to the sea, inland waterbodies are often fragmented or even completely isolated. As a result, sticklebacks became locally adapted to very different conditions in diet, predation pressure, migration range, temperature and water chemistry. For instance, the two major types of inland waters, standing water in lakes and flowing water in rivers, streams or creeks require different morphological and physiological adaptations (e.g., Berner et al., 2014). This divergence, especially between lake and river sticklebacks, within a comparatively short evolutionary period has fueled research in evolutionary biology. Accordingly, numerous traits have been studied in sticklebacks of these two habitat types, especially in interconnected water systems where no physical barriers but only ecological speciation prevent migration and thus gene flow (Thompson et al., 1997, Reusch et al., 2001, Hendry et al., 2002, Hendry et al., 2009, Eizaguirre et al., 2012a, Scharsack et al., 2012, Lenz et al., 2013 and Feulner et al., 2015).

Comparisons of sticklebacks from lakes and rivers revealed differences in the number and types of gill rakers (Lavin and McPhail, 1985, Hendry and Taylor, 2004, Berner et al., 2011, Kaeuffer et al., 2012 and Ravinet et al., 2013), lateral plates (Lavin and McPhail, 1985, Bjaerke et al., 2010 and Berner et al., 2014), general body shape (Reimchen et al., 1985, Lavin and McPhail, 1993, Hendry et al., 2002, Sharpe et al., 2008, Aguirre, 2009 and Berner et al., 2014), mating preferences and reproductive behavior (Rushbrook and Barber, 2008, Raeymaekers et al., 2009, Raeymaekers et al., 2010, Eizaguirre et al., 2011, Moser et al., 2012 and Kaufmann et al., 2014) and general habitat preference (Bolnick et al., 2009). Furthermore, differences in the diversity and abundance of parasite infections were observed between lake and river sticklebacks (e.g., Kalbe et al., 2002 and Scharsack et al., 2007a).

1.2. Parasites as fuel for adaptation

A major selective force in every natural environment is interaction with the sympatric macroparasite fauna. In three-spined sticklebacks, differences in parasite fauna were observed on different scales: within lakes, between benthic and limnetic sticklebacks (MacColl, 2009), at different salinity levels (Zander, 2007), different water temperatures (Karvonen et al., 2013) or between lakes on small geographical scales (de Roij and MacColl, 2012). In this line of research, field studies revealed that intensity and diversity of parasite infections in sticklebacks depend on the habitat of origin and show distinct patterns across habitats (Kalbe et al., 2002). Potential parasite-induced mortalities were attributed rather to co-infections by different parasite species than to individual species (Bråten, 1966 and Kalbe et al., 2002), illustrating how difficult it is to disentangle fitness effects of parasite infections. Accordingly, selective pressure exerted by parasites has to be evaluated in the light of the respective environmental conditions which influence parasite communities through the availability of suitable hosts, transmission and life cycle completion rates.