Punctual ecological changes rather than global factors drive species diversification and the evolution of wing phenotypes in Morpho butterflies

Assessing the relative importance of geographical and ecological drivers of evolution is paramount to understand the diversification of species and traits at the macroevolutionary scale. Here, we use an integrative approach, combining phylogenetics, biogeography, ecology, and quantified phenotypes to investigate the drivers of both species and phenotypic diversification of the iconic Neotropical butterfly genus Morpho. We generated a time-calibrated phylogeny for all known species and inferred historical biogeography. We fitted models of time-dependent (accounting for rate heterogeneity across the phylogeny) and paleoenvironment-dependent diversification (accounting for global effect on the phylogeny). We used geometric morphometrics to assess variation of wing size and shape across the tree, and investigated their dynamics of evolution. We found that the diversification of Morpho is best explained when considering multiple independent diversification dynamics across the tree, possibly associated with lineages occupying different microhabitat conditions. First, a shift from understory to canopy was characterized by an increased speciation rate partially coupled with an increasing rate of wing shape evolution. Second, the occupation of dense bamboo thickets accompanying a major host-plant shift from dicotyledons towards monocotyledons was associated with a simultaneous diversification rate shift and an evolutionary “jump” of wing size. Our study points to a diversification pattern driven by punctual ecological changes instead of a global driver or biogeographic history.

A reversal in sensory processing accompanies ongoing ecological divergence and speciation in Rhagoletis pomonella

Changes in behaviour often drive rapid adaptive evolution and speciation. However, the mechanistic basis for behavioural shifts is largely unknown. The tephritid fruit fly Rhagoletis pomonella is an example of ecological specialization and speciation in action via a recent host plant shift from hawthorn to apple. These flies primarily use specific odours to locate fruit, and because they mate only on or near host fruit, changes in odour preference for apples versus hawthorns translate directly to prezygotic reproductive isolation, initiating speciation. Using a variety of techniques, we found a reversal between apple and hawthorn flies in the sensory processing of key odours associated with host fruit preference at the first olfactory synapse, linking changes in the antennal lobe of the brain with ongoing ecological divergence. Indeed, changes to specific neural pathways of any sensory modality may be a broad mechanism for changes in animal behaviour, catalysing the genesis of new biodiversity.

Nearctic walnut leafminers invade Europe: first Coptodisca lucifluella (Clemens, 1860) and now Coptodisca juglandiella (Chambers, 1874) (Lepidoptera, Heliozelidae)

The Nearctic leafminer of black walnut Coptodisca juglandiella (Chambers, 1874) was found in Hungary and reported as new for Europe. Larvae were found in leafmines on black walnut (Juglans nigra (L.)), white walnut (J. cinerea (L.)) and Arizona walnut (J. major (Torr.)); the latter two Juglans species are new host plant records for C. juglandiella. Mines of Coptodisca lucifluella (Clemens, 1860), another Nearctic invader, were found on leaves of bitternut hickory (Carya cordiformis (Wangenh.) K.Koch) and Caucasian wingnut (Pterocarya fraxinifolia (Lam). Spach.) (a new hostplant record), in addition to common walnut (Juglans regia L.). Interestingly, C. lucifluella is thought to have performed a host plant shift after its introduction into Europe, whereas C. juglandiella apparently did not. Coptodisca juglandiella has three generations in Hungary. The autumn generations of both species produced many more mines than the spring generations. One hymenopteran parasitoid specimen was reared from C. juglandiella. Larvae, mines and adults of C. juglandiella and C. juglandiella can be easily distinguished, differences are presented and illustrated. The genitalia of C. juglandiella are described for the first time.

Bird predation and the host-plant shift by the goldenrod stem galler

Escape from natural enemies may favor the incorporation of a novel host plant into the diet of an herbivorous insect. This scenario has been suggested for the recent host-plant shift by the goldenrod stem galler, Eurosta solidaginis Fitch (Diptera: Tephritidae), from the ancestral host Solidago altissima L. (Compositae) to the derived host Solidago gigantea Ait. In this study, we examined the effects of predation from downy woodpeckers, Picoides pubescens L. (Aves: Picidae), and black-capped chickadees, Parus atricapillus L. (Aves: Paridae), on these two host races of insects at the western edge of their zone of sympatry. Based on a field census, bird predation was concentrated near the cover of trees where S. gigantea tends to occur; few attacks occurred in the open where S. altissima is prevalent. We conducted a field experiment to evaluate the preference of these avian predators for galls of the two host races when differences in the microgeographic distribution, size, and height of galls were controlled. In allopatric sites where only S. gigantea occurs, attacks by birds were 58% more frequent on S. gigantea than on S. altissima galls. Similar results were found for sympatric sites, although the difference in attack was only 26% and not significant. We could find no difference in the toughness of galls or the nutritional value of a larva within the gall (in terms of biomass) to explain avian preference for the S. gigantea host race; however, we found that from 1999 to 2000, the S. gigantea race offered a 27–107% higher reward rate (i.e., the probability that a gall harbored a larva of E. solidaginis) than the S. altissima race. Our studies suggest that avian predators can assess a gall’s content prior to pecking it open, preferring galls that are inhabited by both E. solidaginis larvae and the inquiline predator Mordellistena convicta Leconte (Coleoptera: Mordellidae). It is possible that birds have either learned through experience or evolved through natural selection to choose the more profitable S. gigantea galls. Finally, our results suggest that avian predators act against the maintenance of two distinct host races in the midwestern United States.