Host conservatism, host shifts and diversification across three trophic levels in two Neotropical forests

Abstract

Host–parasite systems have been models for understanding the connection between shifts in resource use and diversification. Despite theoretical expectations, ambiguity remains regarding the frequency and importance of host switches as drivers of speciation in herbivorous insects and their parasitoids. We examine phylogenetic patterns with multiple genetic markers across three trophic levels using a diverse lineage of geometrid moths (Eois), specialist braconid parasitoids (Parapanteles) and plants in the genus Piper. Host–parasite associations are mapped onto phylogenies, and levels of cospeciation are assessed. We find nonrandom patterns of host use within both the moth and wasp phylogenies. The moth–plant associations in particular are characterized by small radiations of moths associated with unique host plants in the same geographic area (i.e. closely related moths using the same host plant species). We suggest a model of diversification that emphasizes an interplay of factors including host shifts, vicariance and adaptation to intraspecific variation within hosts.

Intraspecific phytochemical variation shapes community and population structure for specialist caterpillars

“…These five variables were included in our model with hypothesized relationships (Table 1) that are context dependent and based on previous work with Piper , Eois , and parasitoids (Dyer et al ., 2003, 2004; Brehm et al ., 2007; Connahs et al ., 2009; Smilanich et al ., 2009; Rodríguez‐Castañeda et al ., 2010; Wilson et al ., 2012; Richards et al ., 2015). For example, it was hypothesized that higher relative concentrations of secondary metabolites will decrease the diversity of specialist herbivores as a consequence of higher levels of toxicity (Poelman et al ., 2009; Richards et al ., 2015), and this will positively affect parasitism, because sequestered toxins impair the caterpillars' immune response when consumed (Smilanich et al ., 2009; Richards et al ., 2012).…”

“…As recently as the Pleistocene, multiple, independent clades of Eois caterpillars have undergone geographically localized radiations, in some cases with sister species of Eois in the same geographic area, associated with the same host plant species (Wilson et al ., 2012). This pattern of sympatric sister species utilizing the same resource makes it difficult to assume a framework of ecological divergence in allopatry associated with shifting host species.…”

“…This pattern of sympatric sister species utilizing the same resource makes it difficult to assume a framework of ecological divergence in allopatry associated with shifting host species. However, intraspecific variation in plant chemical defense could contribute to divergence (Wilson et al ., 2012). Piper is chemically defended by a remarkable diversity of secondary compounds that exhibit a broad array of biological activities.…”

Phytochemical diversity drives plant–insect community diversity

“…Ecologists struggle to understand not only the consequences of diversity loss but also how to quantify ecologically relevant dimensions of diversity, including genetic, taxonomic, and functional diversity. Although it has been difficult to measure, phytochemical diversity (i.e., richness and abundance of plant compounds) is a key axis of functional diversity (1) that affects associated trophic levels and is likely driving other aspects of biodiversity (2)(3)(4). Variation in phytochemical or metabolic diversity in plants, which is further downstream than genomic, transcriptomic, or proteomic diversity (5,6), potentially reflects variation in response to a diversity of natural enemies, including specialist and generalist insect herbivores (7,8).…”

The soiil mosaic hypothesis: a synthesis of multi-trophic diversification via soil heterogeneity

“…Divergent selection can result in differences in morphology, behavior, or other phenotypes, potentially leading to genetic isolation between populations comprised of ecologically specialized individuals (Schluter and McPhail 1992, Rundle and Nosil 2005, Matsubayashi et al 2010, Soria-Carrasco et al 2014. Research on ecological speciation has benefited from detailed studies of well-understood populations or taxa associated with different resources or habitats (e.g., Schluter and McPhail 1992, Rundle et al 2000, Nosil et al 2008, Matsubayashi et al 2010, Nosil 2012, Soria-Carrasco et al 2014, but there are still many unexplored axes of ecological variation that potentially contribute to diversification (Coley et al 1985, Thompson 2005, Whitham et al 2008. Here, we consider a previously understudied potential source of divergent natural selection: variation in soils and associated effects on phytochemistry and plant and animal community structure.…”