Host Plant Adaptation in Cactophilic Species of theDrosophila buzzatiiCluster: Fitness and Transcriptomics

Abstract

Host plant shifts in herbivorous insects often involve facing new environments that may speed up the evolution of oviposition behavior, performance related traits, morphology and, incidentally, reproductive isolation. In the genus Drosophila, cactophilic species of the repleta group include emblematic species in the study of the evolution of host plant utilization. The South American D. buzzatii and its sibling D. koepferae are a model system for the study of differential host plant use. Though these species exhibit a certain degree of niche overlap, the former breeds primarily on decaying cladodes of Opuntia cacti while the D. koepferae main hosts are columnar cacti of the genus Trichocereus. Opuntia sulphurea and T. terscheckii are the among the main hosts in nature. These cacti differ in ecological (spatial and temporal predictability) and chemical characteristics. Particularly relevant is the presence of toxic alkaloids in T. terscheckii. Studies of the effects of these cacti and alkaloids revealed the remarkable impact on oviposition behavior, viability, developmental time, wing morphology, mating success and developmental stability in both species. Recent whole-genome expression studies showed that expression profiles are massively affected by the rearing cactus, and that the presence of alkaloids is the main factor modulating gene expression in D. buzzatii. Functional enrichment analysis indicated that differentially expressed genes are related to detoxification processes and stress response; though genes involved in development are an important part of the transcriptomic response. The implications of our studies in the evolution of host plant use in the repleta group are discussed.

What does mitogenomics tell us about the evolutionary history of theDrosophila buzzatiicluster (repletagroup)

“…The adoption of decaying cacti as breeding sites occurred more than once in the evolutionary history of Drosophilidae [25, 26] and is considered a key innovation in the diversification and the invasion of American deserts by species of the Drosophila repleta group ( repleta group from hereafter) [25]. Most species of this group are capable of developing in necrotic cactus tissues while feeding upon cactophilic yeasts associated to the decaying process [27–34].…”

“…The former is an ensemble of seven closely related species, D. antonietae [41], D. borborema [42], D. buzzatii [43], D. gouveai [41], D. koepferae [44], D. serido [42], and D. seriema [45]. All species are endemic to South America (Fig 1), except the semi-cosmopolitan D. buzzatii that reached a wide distribution following human mediated dispersion of prickly pears of the genus Opuntia (Caryophillales, Cactaceae) in historical times [34, 46, 47]. These species inhabit open areas of sub-Amazonian semidesertic and desertic regions of South America, where flies use necrotic cactus tissues as obligatory feeding and breeding resources [34, 48].…”

“…All species are endemic to South America (Fig 1), except the semi-cosmopolitan D. buzzatii that reached a wide distribution following human mediated dispersion of prickly pears of the genus Opuntia (Caryophillales, Cactaceae) in historical times [34, 46, 47]. These species inhabit open areas of sub-Amazonian semidesertic and desertic regions of South America, where flies use necrotic cactus tissues as obligatory feeding and breeding resources [34, 48]. Regarding host plant utilization, D. buzzatii is an Opuntia specialist [30], a condition considered as ancestral [25].…”

“…Regarding host plant utilization, D. buzzatii is an Opuntia specialist [30], a condition considered as ancestral [25]. However, D. buzzatii has also been recovered from necrotic columnar cacti [34]. The remaining species are mainly columnar dwellers though D. antonietae , D. serido and D. koepferae can also emerge marginally from rotting prickly pears [48].…”

“…Species of the buzzatii cluster are almost indistinguishable by external morphology, however, differences in the morphology of male intromittent organ (aedeagus) and polytene chromosomes banding patterns provide clues to species identification (reviewed in [34, 47, 50]). The cluster has been divided into two groups based on aedeagus morphology, the first includes D. buzzatii and the remaining species compose the so-called Drosophila serido sibling set - serido sibling set from hereafter-[47].…”