Is ecological speciation a major trend in aphids? Insights from a molecular phylogeny of the conifer-feeding genus Cinara

Abstract

IntroductionIn the past decade ecological speciation has been recognized as having an important role in the diversification of plant-feeding insects. Aphids are host-specialised phytophagous insects that mate on their host plants and, as such, they are prone to experience reproductive isolation linked with host plant association that could ultimately lead to species formation. The generality of such a scenario remains to be tested through macroevolutionary studies. To explore the prevalence of host-driven speciation in the diversification of the aphid genus Cinara and to investigate alternative modes of speciation, we reconstructed a phylogeny of this genus based on mitochondrial, nuclear and Buchnera aphidicola DNA sequence fragments and applied a DNA-based method of species delimitation. Using a recent software (PhyloType), we explored evolutionary transitions in host-plant genera, feeding sites and geographic distributions in the diversification of Cinara and investigated how transitions in these characters have accompanied speciation events.ResultsThe diversification of Cinara has been constrained by host fidelity to conifer genera sometimes followed by sequential colonization onto different host species and by feeding-site specialisation. Nevertheless, our analyses suggest that, at the most, only half of the speciation events were accompanied by ecological niche shifts. The contribution of geographical isolation in the speciation process is clearly apparent in the occurrence of species from two continents in the same clades in relatively terminal positions in our phylogeny. Furthermore, in agreement with predictions from scenarios in which geographic isolation accounts for speciation events, geographic overlap between species increased significantly with time elapsed since their separation.ConclusionsThe history of Cinara offers a different perspective on the mode of speciation of aphids than that provided by classic models such as the pea aphid. In this genus of aphids, the role of climate and landscape history has probably been as important as host-plant specialisation in having shaped present-day diversity.

Buchnera has changed flatmate but the repeated replacement of co‐obligate symbionts is not associated with the ecological expansions of their aphid hosts

“…DNA was extracted, amplified and sequenced as in previous studies (Jousselin et al . ). A total of seventy‐five specimens were newly sequenced for this study, while the other sequences were retrieved from GenBank (Appendix S1, Supporting information).…”

“…We assigned character states by combining information available in the literature for each recognized Cinara species (Blackman & Eastop ; Jousselin et al . ) and information recorded from the field in the course of aphid sampling. We did not explore the effect of aphid life cycle nor the association of aphids with ants as all Cinara species are monoecious and almost all are attended by ants.…”

Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiont‐rich aphid genus

“…Total genomic DNA was extracted from whole individuals with the same extraction kit as used for the procedure described above. In parallel, we used DNA extracts from our previous phylogenetic investigations of the genus Cinara (Jousselin et al . ). These extracts were obtained with the EZ‐10 96‐Well Plate Genomic DNA Extraction Kit, Animal Samples (Bio Basic Inc., ON, Canada), in 2012, from individuals from the same aphid colonies as used in the other two protocols.…”

European species of the aphid genus Eulachnus Del Guercio, 1909 (Hemiptera: Aphididae: Lachninae): revision and molecular phylogeny

“…Two first of them are formed in general by long-haired species from the "agilis" group and the short-haired species like E. brevipilosus and E. cembrae, and the individual position of E. nigricola most probably due to the abovementioned characters of this species. In comparison with the COI tree, the ITS2 phylogeny shows that studied species belonging to morphologically different groups are members of one, probably young and not strongly differentiated genus of aphids associated with one plant genus and one part of the plants which, in Lachninae, are known as hosts only in the Cinara subgenus Schizolachnus and, with one exception in the genus Essigella, in opposition to species from other Cinara subgenera and other Lachninae genera (Favret & Voegtlin 2004b;Jousselin et al 2013;Mroz et al 2015;Chen et al 2016). The relatively young age of the genus and close relations between particular species in subgroups could be the reason for the observed lack of congruence between mitochondrial and nuclear gene trees.…”