Rampant host‐ and defensive phenotype‐associated diversification in a goldenrod gall midge

Abstract

Natural selection can play an important role in the genetic divergence of populations and their subsequent speciation. Such adaptive diversification, or ecological speciation, might underlie the enormous diversity of plant-feeding insects that frequently experience strong selection pressures associated with host plant use as well as from natural enemies. This view is supported by increasing documentation of host-associated (genetic) differentiation in populations of plant-feeding insects using alternate hosts. Here, we examine evolutionary diversification in a single nominal taxon, the gall midge Asteromyia carbonifera (O.S.), with respect to host plant use and gall phenotype. Because galls can be viewed as extended defensive phenotypes of the midges, gall morphology is likely to be a reflection of selective pressures by enemies. Using phylogenetic and comparative analyses of mtDNA and nuclear sequence data, we find evidence that A. carbonifera populations are rapidly diversifying along host plant and gall morphological lines. At a broad scale, geography explains surprisingly little genetic variation, and there is little evidence of strict co-cladogenesis with their Solidago hosts. Gall morphology is relatively labile, distinct gall morphs have evolved repeatedly and colonized multiple hosts, and multiple genetically and morphologically distinct morphs frequently coexist on a single host plant species. These results suggest that Asteromyia carbonifera is in the midst of an adaptive radiation driven by multitrophic selective pressures. Similar complex community pressures are likely to play a role in the diversification of other herbivorous insect groups.

Taxonomy and phylogeny of theAsphondyliaspecies (Diptera: Cecidomyiidae) of North American goldenrods: challenging morphology, complex host associations, and cryptic speciation

“…Because they are easy to manipulate in field and greenhouse experiments, goldenrods have served as model systems for numerous studies on evolutionary and ecological aspects of speciation and tritrophic interactions (e.g. Abrahamson & Weis, ; Stireman et al ., , , ; Crutsinger, Cadotte & Sanders, ; Dixon, Craig & Itami, ; Wise, Cole & Carr, ; Craig et al ., ; Hakes & Cronin, ). Of the 50 or so insect species known to induce galls on goldenrods, about 30 species are cecidomyiids.…”

“…Gall midges (Diptera: Cecidomyiidae) are excellent models for studying the importance and context of such shifts because of the intimate nature of their relationships with their host plants, and because closely related groups of gall midges are known to diversify through shifts between hosts and through shifts between organs within a host‐plant species (e.g. Jones, Gagné & Barr, ; Hawkins, Goeden & Gagné, ; Joy & Crespi, ; Stireman, Devlin & Abbot, ).…”

Genetically differentiated races and speciation-with-gene-flow in the sunflower maggot, Strauzia longipennis

“…The result is the formation of partially isolated races, presumed to be an early step along the so-called ''speciation continuum'' (Mallet 2008). Genetically differentiated races within morphologically defined species have also been found to coexist on a single plant species, particularly among taxa that have recently undergone adaptive radiations (Marsteller et al 2009;Stireman et al 2012). Further, recent empirical and theoretical work demonstrating that populations can diverge even in the face of effective migration (Nosil 2008;Nosil and Feder 2012), as well as new information about the permeability of genomes to between-lineage gene flow (Turner et al 1999;Michel et al 2010;Gompert et al 2010) both suggest that persistent hybridization between closely related lineages may occur without leading to lineage fusion or breakdown of reproductive barriers.…”

Climate-Driven Reshuffling of Species and Genes: Potential Conservation Roles for Species Translocations and Recombinant Hybrid Genotypes

“…Levels of speciation and adaptation often differ within a single species [ 117 , 254 , 257 ]. The determination of where species boundaries occur biologically is even more difficult to determine because of hybrid introgression, genetic porosity, and the blurring of taxonomic categories that include subspecies [ 30 , 258 ], host races [ 259 , 260 , 261 ], polymorphisms [ 262 , 263 ], cryptic species [ 101 , 264 , 265 ] and even “hybrid species” [ 26 , 27 , 68 , 69 , 100 , 101 , 120 , 121 , 266 , 267 ].…”