Spatial variation in defensive traits is common in many antagonistic interactions [1-3]. The geographic mosaic theory of coevolution suggests that variation in ecological factors may underlie this patchiness in the phenotypic outcome of interactions, resulting in cold and hotspots of coevolution [2,4,5]. Despite evidence for coevolutionary cold and hotspots, very little evidence exists on how ecological conditions may enhance or constrain coevolution between antagonists. One current model suggests that coevolution might be related to gradients in resource productivity [6], with hotspots of coevolutionary selection associated with areas of high prey abundance. In specialist predator-prey interactions, predators have the greatest influence on prey phenotypes in geographic areas where the prey is most abundant whereas the predator exerts weaker selection in areas where prey are less abundant. Conditions of high prey abundance can occur when the abiotic environment is most favorable for prey metabolism or prey resources are of high quality/abundance. In the current study, we examine the effect of abiotic and biotic factors on spatial variation in the evolution of putative defensive traits of the freshwater snail Mexipyrgus churinceanus.
Mexipyrgus churinceanus as well as its polymorphic fish predator Herichthys minckleyi are endemic to the isolated Cuatro Ciénegas valley in the Mexican Chihuahuan desert (Fig. 1) and exhibit putatively co-evolved phenotypes [7-9]. These phenotypes may currently be coevolving because Mexipyrgus exhibits striking examples of morphological differentiation in shell morphology and pigmentation among habitats [[10-12]; Fig. 2]. Herichthys minckleyi is also unusual because this cichlid fish exhibits two alternative pharyngeal jaw morphologies [[13,14]; Fig. 2]. In "papilliform" H. minckleyi, the gill arches are modified into a gracile pharyngeal jaw and this morph is specialized to shred aquatic plants and detritus [15]. Alternatively, "molariforms" possess enlarged crushing molariform teeth and robust pharyngeal muscles [16] and are extremely proficient at crushing M. churinceanus [15]. Molariform cichlids are the primary snail-crushing predator in Cuatro Ciénegas.
Given considerable spatial variation in shell pigmentation and morphology, we hypothesize that several types of snail defenses have evolved in response to predation by molariform H. minckleyi. For instance, cryptic coloration against different benthic substrates may minimize detection by molariform cichlids. The abundance of emergent aquatic vegetation, such as Nymphaea water lilies, is highly variable in these aquatic habitats, and may be primarily responsible for the coloration of the substrate. Darker substrates dominate in areas with dense Nymphaea stands and light, marl-colored substrates occur in the absence of Nymphaea (Fig. 2). Unpigmented M. churinceanus may be more cryptic and common in habitats without Nymphaea whereas, in heavily vegetated habitats, snails with extensive shell pigmentation may dominate because they effectively match these darker substrates.
Shell pigmentation is not the only defense M. churinceanus may exhibit in response to molariform predation. Crushing resistance is likely the most functionally important component of shell defense against molariform H. minckleyi [15] because it allows snails to resist predation once detected. Because previous studies of defensive traits in gastropods indicate that shell size and shape both influence crushing resistance [17,18], we first examine whether size or shape is a better predictor of variation in crushing resistance. Next, we assess potential causes of spatial divergence in Mexipyrgus defensive traits. The abiotic characteristics of Cuatro Ciénegas may be unusually favorable for the production of elaborate snail shells. The spring-fed habitats are geothermally heated and high in dissolved minerals [7]. For mollusks, higher temperatures permit elaboration of their shells because calcium carbonate is less soluble in warmer water [19,20]. Maintaining robust shells is also physiologically cheap in constant aquatic environments with elevated mineral content [20,21] especially since Ca++ availability is correlated with the availability of other dissolved minerals in Cuatro Ciénegas [22]. We examined whether spatial variation in temperature and conductivity are positively correlated with snail defensive traits.
Alternatively, variation in shell strength might be primarily a response to biotic influences. We address whether spatial variation in snail defenses is associated with two biotic factors: molariform frequency and resource productivity. If molariform H. minckleyi predation is the primary force driving spatial variation in snail defensive traits, we might predict that snail populations with higher frequencies of molariforms should exhibit greater crushing resistance and pigmentation. We also assess whether habitats with greater primary productivity promote escalation of defensive snail phenotypes. We determine whether, in habitats with greater abundance of Nymphaea, Mexipyrgus exhibits more shell pigmentation and crushing resistance. For Mexipyrgus, variation in resource productivity is likely to be driven by the abundance of Nymphaea because in habitats with greater primary productivity, there is a greater abundance of bacteria and fungi in the soft substrates in which Mexipyrgus feeds (Johnson, unpublished results). Increased resource availability probably allows greater investment in costly shell material, leading to the prediction that hotspots may occur in areas with greater food resources for snails.
A critical assumption of these population-based measures of phenotypic divergence is that they are statistically independent. This assumption may be violated because nearby snail populations may experience similar predation pressure because cichlids are more mobile than these brooding snails. To address this issue we assess whether the similarity of shell defensive traits among nearby populations can be attributed to either geographic proximity or genetic similarity [23-25]. Genealogical relationships within species based on geographic and genetic distances among populations can be used in conjunction with spatial autocorrelation approaches to determine whether defensive structures of nearby populations are positively autocorrelated. A lack of spatial autocorrelation suggests that defenses are distributed in a mosaic-like fashion across the landscape. If phenotypic divergence in crushing resistance and pigmentation is the result of predator-prey interactions with H. minckleyi, and this divergence occurs at very small spatial scales in a geographically mosaic fashion, we predict there will be no significant positive autocorrelation at small spatial and genetic distances. In the current study, we determine genetic distances between snail populations from a previously published study of mtDNA sequence variation in Mexipyrgus [26].
We address three questions concerning the evolution of defenses in Mexipyrgus. First, we examine spatial variation in two putative defensive traits, crushing resistance and shell pigmentation. Then, we tested whether abiotic or biotic variables account for spatial patterns of crushing resistance and shell pigmentation. Finally, we determine whether variation in primary productivity accounts for small-scale variation in these defensive traits.
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