Evo Edu Outreach (2010) 3:26–31 DOI 10.1007/s12052-009-0191-7 ORIGINAL SCIENTIFIC ARTICLE Arms Race Coevolution: The Local and Geographical Structure of a Host–Parasite Interaction Rodrigo Medel & Marco A. Mendez & Carmen G. Ossa & Carezza Botto-Mahan Published online: 19 December 2009 # Springer Science+Business Media, LLC 2009 Abstract Consideration of complex geographic patterns of dence indicate that arms-race coevolution is an ongoing reciprocal adaptation has provided insight into new features phenomenon that occurs in the global system of of the coevolutionary process. In this paper, we provide interconnected populations. ecological, historical, and geographical evidence for coevo- lution under complex temporal and spatial scenarios that Keywords Geographic mosaic of coevolution . Adaptation . include intermittent selection, species turnover across Host–parasite . Mistletoe . Cactus . Chile . Natural selection localities, and a range of trait match/mismatch across populations. Our study focuses on a plant host–parasitic plant interaction endemic to arid and semiarid regions of Introduction Chile. The long spines of Chilean cacti have been suggested to evolve under parasite-mediated selection as a Host–parasite relationships have long attracted the attention first line of defense against the mistletoe Tristerix aphyllus. of ecologists and evolutionary biologists because reciprocal The mistletoe, in turn, has evolved an extremely long adaptive responses may coevolve as a result of the morphological structure that emerges from the seed antagonistic interaction. Implicit in most models of endosperm (radicle) to reach the host cuticle. When spine host–parasite coevolution is the idea that host character- length was traced along cactus phylogenies, a significant istics providing defense against parasitism are adaptive and association between spine length and parasitism was evolve under parasite-mediated selection, and infection detected, indicating that defensive traits evolved in high parasite traits, in turn, evolve as a response to the host correspondence with the presence or absence of parasitism defensive traits evolved by host populations. In spite of its in two cactus lineages. Assessment of spine-radicle match- apparent simplicity, this idea has been difficult to evaluate ing across populations revealed a potential for coevolution empirically, and coadaptation of host and parasite traits is in 50% of interaction pairs. Interestingly, hot spots for usually assumed rather than demonstrated. One possible coevolution did not distribute at random across sites. On the reason for this is that reciprocal selection is not an all-or- contrary, interaction pairs showing high matching values none phenomenon that necessarily occurs in the overall occur mostly in the northern distribution of the interaction, range of localities where host and parasite coexist. This suggesting a geographical structure for coevolution in this somewhat restricted and local view of coevolution has been system. Only three sampled interaction pairs were so recently expanded to a geographical perspective that takes mismatched that reciprocal selection could not occur given into account a broader range of scenarios than previously current trait distributions. Overall, different lines of evi- considered. For example, at any point in space and time, interacting populations may occupy any position within the : : : R. Medel (*) M. A. Mendez C. G. Ossa C. Botto-Mahan range of the coevolutionary race depending on the Departamento de Ciencias Ecológicas, Facultad de Ciencias, temperature of populations: from the early stages of Universidad de Chile, escalation with a high rate of reciprocal selection Casilla 653, Santiago, Chile (hotspots), to low reciprocal selection and cost-induced e-mail: [email protected] de-escalation (coldspots). Because a variety of historical, Evo Edu Outreach (2010) 3:26–31 27 geographical, and ecological factors may influence the tions and experiments to identify: (a) the species with coevolutionary process, it is exceedingly difficult to draw potential to exhibit arms-race coevolution, (b) the inferences about the coevolutionary dynamics of interspe- phenotypic traits involved in reciprocal selection, that cific interactions through the examination of one or a few is, those traits with a clear functional value that localities at a single time. This perspective has been influence the distribution of mortality or fecundity on articulated into what has been called the Geographical each population, and (c) the temporal dynamics of Mosaic of Coevolution Theory (Thompson 1994, 2005), selection acting on the relevant functional traits. Second, which takes explicitly into account the inherent complexity we will use a phylogenetic approach to determine: (a) of local communities, the ample temporal and spatial the pattern of trait evolution on a broad temporal scale variation in species composition and interactions, and the and (b) the extent to which trait evolution is associated heterogeneity in the magnitude, direction, and shape of with the presence or absence of the interacting antag- reciprocal selection across localities. onistic species. Third, we will evaluate the actual Arms race is a specific form of coevolution that is geographic mosaic by (a) assessing the degree of characterized by escalating levels of defense and counter- matching and mismatching of coevolved traits across defense in antagonistic interactions. However, arms-race localities and (b) examining a potential regional struc- coevolution does not necessarily imply an endless ture of trait matching/mismatching in a multispecific increase in defense and counterdefense phenotypes. For context. Together, these approaches to coevolutionary example, the geographic structure of the interaction may analysiscanhelpustounderstandtheextenttowhich prevent the relentless escalation through the acquisition of geographic selection mosaics have shaped trait distribu- new defense mechanisms that may replace the original tion across landscapes in this model system. one in some populations (e.g., Benkman 1999; Benkman et al. 2003). Gene flow across localities may arm host species with a battery of possibilities including the Natural History and the Phenotypic Interface original defense, the new defense, or a combination of both, probably depending on the level of overlapping The parasitic habit in plants is represented by more than between host and parasite populations (Nuismer et al. 3,000 species distributed in 16 families (Kuijt 1969; 2003) Similarly, gene flow between hotspots and cold- Musselman and Press 1995). In total, parasitic plants spots will slow the rate of escalation in the global system represent about 1% of the total species of angiosperms, of interconnected populations. and Loranthaceae is the most diversified family with ca. The arms race model for host–parasite interactions 700 species distributed in 22 genera around the world makes several specific predictions (Thompson 1994, 2005): (Molau 1995). The family Loranthaceae diversified in warm climates, probably in closed forests in the mid- 1. Local populations of the parasite are adapted to the Cretaceous about 70 million years ago (Barlow 1983). The least defended of their potential local host assemblage. South American genus Tristerix consists of 11 mistletoe 2. Parasite hierarchies of infection vary geographically, species distributed in the west margin of the continent. indicating host alternation across localities. Tristerix aphyllus is a peculiar mistletoe endemic to the 3. Some uninfected hosts exhibit high levels of defense, arid and semiarid regions of Chile that, unlike all other providing correlative evidence for past adaptive or species of Loranthaceae, has leaves reduced to minute anachronic traits to the interaction that have not yet scales (Kuijt 1969, 1988;Fig.1a). The leafless condition been lost. of T. aphyllus has been hypothesized to represent a 4. Some host populations may show low levels of derived adaptation to its peculiar life history that, unlike defense, indicating that (1) the species is new to the all other species in the Loranthaceae, includes cacti as the antagonistic interaction or (2) the species is a host that only host species (Mauseth 1991). T. aphyllus currently lost its defense as the parasite focused on an alternative parasitizes several columnar cacti of the genera Echinopsis host species. (Trichocereus)andEulychnia. Different lines of geologi- 5. Host populations may show variable defense levels cal, climatic, and biogeographical evidence suggest the across localities, indicating different levels of defense association Tristerix-cactimayhaveoriginatedaboutfive ratcheting in different community contexts. million years ago (Medel et al. 2002). Since then, Tristerix In this paper, we will focus on a specific host- has probably spread by including an increasing number of parasite relationship to illustrate some elements of the cactus species as hosts, adopting its current distribution in arms race model in the context of the Geographical strict dependence upon cactus distribution. In Chile, the Mosaic of Coevolution Theory. To this end, we will use current distribution of the host–parasite interaction three approaches. First, we will use ecological observa- extends from 27°S to 35°S. 28 Evo Edu Outreach (2010) 3:26–31 Fig. 1 The infection cycle in the cactus–mistletoe system. The fruits of the holoparasitic mistletoe Tristerix aphyllus (a) is one of the few feeding resources for