Arms Race Coevolution: The Local and Geographical Structure of a Host–Parasite Interaction
© Springer Science+Business Media, LLC 2009
Published: 19 December 2009
Consideration of complex geographic patterns of reciprocal adaptation has provided insight into new features of the coevolutionary process. In this paper, we provide ecological, historical, and geographical evidence for coevolution under complex temporal and spatial scenarios that include intermittent selection, species turnover across 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 Chile. The long spines of Chilean cacti have been suggested to evolve under parasite-mediated selection as a first line of defense against the mistletoe Tristerix aphyllus. The mistletoe, in turn, has evolved an extremely long morphological structure that emerges from the seed endosperm (radicle) to reach the host cuticle. When spine length was traced along cactus phylogenies, a significant association between spine length and parasitism was detected, indicating that defensive traits evolved in high correspondence with the presence or absence of parasitism in two cactus lineages. Assessment of spine-radicle matching across populations revealed a potential for coevolution in 50% of interaction pairs. Interestingly, hot spots for coevolution did not distribute at random across sites. On the contrary, interaction pairs showing high matching values occur mostly in the northern distribution of the interaction, suggesting a geographical structure for coevolution in this system. Only three sampled interaction pairs were so mismatched that reciprocal selection could not occur given current trait distributions. Overall, different lines of evidence indicate that arms-race coevolution is an ongoing phenomenon that occurs in the global system of interconnected populations.
Host–parasite relationships have long attracted the attention of ecologists and evolutionary biologists because reciprocal adaptive responses may coevolve as a result of the antagonistic interaction. Implicit in most models of host–parasite coevolution is the idea that host characteristics providing defense against parasitism are adaptive and evolve under parasite-mediated selection, and infection parasite traits, in turn, evolve as a response to the host defensive traits evolved by host populations. In spite of its apparent simplicity, this idea has been difficult to evaluate empirically, and coadaptation of host and parasite traits is usually assumed rather than demonstrated. One possible reason for this is that reciprocal selection is not an all-or-none phenomenon that necessarily occurs in the overall range of localities where host and parasite coexist. This somewhat restricted and local view of coevolution has been recently expanded to a geographical perspective that takes into account a broader range of scenarios than previously considered. For example, at any point in space and time, interacting populations may occupy any position within the range of the coevolutionary race depending on the temperature of populations: from the early stages of escalation with a high rate of reciprocal selection (hotspots), to low reciprocal selection and cost-induced de-escalation (coldspots). Because a variety of historical, geographical, and ecological factors may influence the coevolutionary process, it is exceedingly difficult to draw inferences about the coevolutionary dynamics of interspecific interactions through the examination of one or a few localities at a single time. This perspective has been articulated into what has been called the Geographical Mosaic of Coevolution Theory (Thompson 1994, 2005), which takes explicitly into account the inherent complexity of local communities, the ample temporal and spatial variation in species composition and interactions, and the heterogeneity in the magnitude, direction, and shape of reciprocal selection across localities.
Arms race is a specific form of coevolution that is characterized by escalating levels of defense and counterdefense in antagonistic interactions. However, arms-race coevolution does not necessarily imply an endless increase in defense and counterdefense phenotypes. For example, the geographic structure of the interaction may prevent the relentless escalation through the acquisition of new defense mechanisms that may replace the original 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 original defense, the new defense, or a combination of both, probably depending on the level of overlapping between host and parasite populations (Nuismer et al. 2003) Similarly, gene flow between hotspots and coldspots will slow the rate of escalation in the global system of interconnected populations.
Local populations of the parasite are adapted to the least defended of their potential local host assemblage.
Parasite hierarchies of infection vary geographically, indicating host alternation across localities.
Some uninfected hosts exhibit high levels of defense, providing correlative evidence for past adaptive or anachronic traits to the interaction that have not yet been lost.
Some host populations may show low levels of defense, indicating that (1) the species is new to the antagonistic interaction or (2) the species is a host that lost its defense as the parasite focused on an alternative host species.
Host populations may show variable defense levels across localities, indicating different levels of defense ratcheting in different community contexts.
In this paper, we will focus on a specific host-parasite relationship to illustrate some elements of the arms race model in the context of the Geographical Mosaic of Coevolution Theory. To this end, we will use three approaches. First, we will use ecological observations and experiments to identify: (a) the species with potential to exhibit arms-race coevolution, (b) the phenotypic traits involved in reciprocal selection, that is, those traits with a clear functional value that influence the distribution of mortality or fecundity on each population, and (c) the temporal dynamics of selection acting on the relevant functional traits. Second, we will use a phylogenetic approach to determine: (a) the pattern of trait evolution on a broad temporal scale and (b) the extent to which trait evolution is associated with the presence or absence of the interacting antagonistic species. Third, we will evaluate the actual geographic mosaic by (a) assessing the degree of matching and mismatching of coevolved traits across localities and (b) examining a potential regional structure of trait matching/mismatching in a multispecific context. Together, these approaches to coevolutionary analysis can help us to understand the extent to which geographic selection mosaics have shaped trait distribution across landscapes in this model system.
Natural History and the Phenotypic Interface
The parasitic habit in plants is represented by more than 3,000 species distributed in 16 families (Kuijt 1969; Musselman and Press 1995). In total, parasitic plants represent about 1% of the total species of angiosperms, and Loranthaceae is the most diversified family with ca. 700 species distributed in 22 genera around the world (Molau 1995). The family Loranthaceae diversified in warm climates, probably in closed forests in the mid-Cretaceous about 70 million years ago (Barlow 1983). The South American genus Tristerix consists of 11 mistletoe species distributed in the west margin of the continent.
The infection by T. aphyllus spreads from one host to another through the Chilean mockingbird Mimus thenca (Mimidae), the only bird species responsible for disseminating the seeds of the mistletoe (Fig. 1b). The bird swallows whole ripe fruits and defecates the mucilaginous seeds intact (Martinez del Río et al. 1995). Seed deposition upon cacti is often aggregated and occurs especially on short-spined and previously parasitized individuals (Medel et al. 2004). Once defecated by the bird, the seeds often adhere to the spines of cacti and elongate a reddish morphological structure that protrudes from the seed endosperm (radicle, hereafter) that grows up to eight weeks (Fig. 1c) or until making contact with the epidermis of the cactus to form a morphological zone of contact (Fig. 1d) from which several filaments penetrate into cactus tissues through stomatal openings (see morphological details in Mauseth et al. 1984, 1985). Once inside the cactus, the plant grows for 18 months before emerging from the cactus surface as a red inflorescence to repeat the cycle (Botto-Mahan et al. 2000; Fig. 1e).
The Phylogenetic Structure of the Coevolving System
T. aphyllus currently parasitizes some but not all Echinopsis and Eulychnia species in Chile. For instance, several columnar cactus species currently inhabit places outside the geographical range of the parasitic plant, which suggests they have not had a history of association with the mistletoe. This geographical setting provides a useful scenario in which to evaluate the historical association of spine length with parasitism and to perform tests for correlated evolution in a phylogenetic context. Because phylogenies permit us to track the distribution of traits from a large-scale perspective, it is possible to understand the pathways followed by the coevolving interaction to its current geographical configuration.
In conclusion, phylogenetic evidence indicates that (1) host species that present high levels of infection at present tend to show long spines, (2) the host species living outside the distributional range of the mistletoe at present have shorter spines than their relatives probably because, unlike parasitized species, they have never been involved in arms-race coevolution, and (3) the pattern is consistent in host species belonging to different genera. All this evidence provides support to the idea that host–parasite coevolution occurs in a changing multispecific context across localities, therefore verifying a critical premise of the Geographic Mosaic of Coevolution Theory.
Matches and Mismatches Across Populations
We have presented different lines of evidence for arms-race coevolution in the mistletoe–cactus system. Identification of the relevant traits for the interaction has permitted an exploration of a range of questions that include local, phylogenetic, and geographical perspectives. Taken together, all the evidence indicates a phenomenon far more complex than previously thought. Intermittent local selection combined with a high host species turnover across localities indicates a very dynamic coevolutionary process that is reflected in the variable levels of host-parasite matching and mismatching at the regional scale. In spite of this community complexity, however, the long-term phylogenetic signal indicates a strong association between host defensive characters and parasitism, indicating that the mistletoe is responsible for the extremely long spines presented by some Chilean columnar cacti, and cacti have promoted the extremely long radicle in the mistletoe. Overall, these evidences indicate that regardless of the inherent community complexity at each locality, arms-race coevolution is an ongoing process in the global system. Current work on the phylogeographic structure of the interaction will help us to understand the genetic and historical determinants of the cactus–mistletoe coevolving system across landscapes.
We thank Paula Caballero, Mildred Ehrenfeld, Wilfredo Gonzáles, Carlos Martinez del Río, Talía del Pozo, Eric Rivera, Arturo Silva, Eliseo Vergara, and the family Montero Peña for their collaboration in different steps of this research. CONAF IV Region and the personnel of Las Chinchillas National Reserve provided invaluable support during this research. John Thompson and Niles Eldredge made important comments that improved the clarity of this manuscript. This work was funded by grants FONDECYT 1970497, 1010660, PSD 66, and ACT 34/2006 to RM.
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