Pronounced geographic differences in prey defenses are probably common [5,27]. While the unusually high crushing resistance of Mexipyrgus churinceanus in Cuatro Ciénegas and the presence of the molariform cichlids are suggestive of coevolutionary selection [8,15], the current study provides three important insights. First, there is considerable small-scale spatial variation in crushing resistance and pigmentation that exhibits a mosaic distribution with no significant genetic or spatial autocorrelation. Also, there was a significant negative correlation between the frequency of molariforms and both size-adjusted crushing resistance and frequency of shell pigmentation, but no relationship between these defensive traits and the abiotic variables. Lastly, crushing resistance and pigmentation are significantly higher in habitats dominated by aquatic macrophytes.
To address whether prey defenses have evolved independently across the geographic range of Mexipyrgus churinceanus requires an assessment of phenotypic variation and the spatial autocorrelation of these traits among populations at small genetic and geographic distances. There is significant spatial variation in M. churinceanus crushing resistance and pigmentation at small spatial scales suggesting that certain factors may cause this mosaic distribution of snail defensive traits. In paired populations separated by very small linear and genetic distances, elevated crushing resistance occurs in habitats containing extensive Nymphaea stands. Crushing resistance is dramatically lower in light colored substrates lacking Nymphaea. Because Tio Candido and Rio Mesquites populations represent distinct lineages based on mtDNA sequence differentiation [26], it suggests that these represent convergent patterns of increased crushing resistance and tantalizingly suggests these differences may be driven by resource availability. In habitats with greater primary productivity, there is probably greater abundance of bacteria and fungi upon which Mexipyrgus feeds extensively (Johnson, unpublished results). Increased resource availability likely allows greater investment in costly shell material, and experiments that manipulate resource availability to test its effect on Mexipyrgus shell strength would provide a further test of this hypothesis.
Although there is considerable documentation of hotspots and coldspots in coevolved antagonistic interactions, how spatial processes and community composition promote coevolution and generate selection mosaics has received less attention. A recent study of herbivorous weevils and their Camellia host plant indicate that escalation in armaments only occurred in southern latitudes [3]. More northern host populations had reduced resistance but exploitation and damage by weevils was even greater in these populations, suggesting that some unknown ecological factor may constrain resistance in northern host populations. There has been speculation that the exaggerated shell form of Mexipyrgus is the result of coevolutionary interactions between endemic snails and the molluscivorous morph of H. minckleyi [8]. Surprisingly, there was a highly significant negative relationship between molariform frequency and size-adjusted crushing resistance among ten populations, suggesting that molariform fitness declines as snail crushing resistance increases. Molariform cichlids may have a greater fitness advantage in resource-poor environments where snail crushing resistance is lower, and the limited availability of plant material reduces papilliform fitness. In Nymphaea habitats, increased snail crushing resistance may reduce molariform fitness due to increased costs of crushing, while papilliform fitness is higher due to increased availability of plant material for shredding. We plan to experimentally test whether these alternative cichlid morphs have fitness trade-offs in different resource environments, and more quantitatively measure resources available to Mexipyrgus.
Microspatial variation in Mexipyrgus shell pigmentation is also associated with different substrate coloration and there is no evidence of genetic or spatial autocorrelation among populations. In the three geographically-paired populations, snails with pigmented bands were significantly more common in Nymphaea habitats and unbanded snails were more common where the benthic substrate was light and marled- colored. Unbanded snails are probably more cryptic against lighter benthic substrates and banded snails are more cryptic against the darker substrates found in association with Nymphaea. This type of background matching by prey under selection from highly visual predators is common in many organisms [28-30] and experimental evidence that banding patterns are cryptic against different substrate backgrounds would be an interesting line of further research.
The positive relationship between the two snail traits across environments suggest that pigmentation and crushing resistance may represent phenotypically-correlated traits. In resource-poor environments where Nymphaea is absent, investment in crushing resistance may be constrained due to resource limitation, so that crypsis is the most effective defense against molariform predation. We suspect that investment in shell pigmentation is not as costly as having more robust shells, and that snails are capable of inexpensively modifying their pigmentation in Nymphaea habitats to increase crypsis. Whether correlational selection acts on pigmentation patterns and shell strength in these habitats requires a deeper understanding of the phenotypic plasticity in both traits. One hypothesis is that increased pigmentation in these environments does not increase background matching, and pigmentation only increases due to correlational selection on crushing resistance. This hypothesis could be easily refuted if predation success on banded shells is less in Nymphaea habitats. Given evidence for inducible defenses in snails [31-33], we also need to assess the heritability and phenotypic plasticity of crushing resistance and pigmentation.
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