Transcriptomic differences between euryhaline and stenohaline malaria vector sibling species in response to salinity stress

Abstract

Evolution of osmoregulatory systems is a key factor in the transition of species between fresh- and saltwater habitats. Anopheles coluzzii and An. merus are stenohaline and euryhaline malaria vector mosquitoes belonging to a larger group of sibling species, the Anopheles gambiae complex, which radiated in Africa within the last 2 million years. Comparative ecological genomics of these vector species can provide insight into the mechanisms that permitted the rapid radiation of this species complex into habitats of contrasting salinity. Here we use RNA-Seq to investigate gene expression differences between An. coluzzii and An. merus after briefly exposing both young and old larval instars of each species to either saltwater (SW) or freshwater (FW). Our examination aims to identify candidate genes and pathways responsible for the greater SW tolerance of An. merus. Our results are congruent with the ability of gene induction to mediate salinity tolerance, with both species showing increasing amounts of differential gene expression between SW and FW as salt concentrations increase. Besides ion transporters such as AgAE2 that may serve as effectors for osmoregulation, we also find mitogen activated protein kinases that may serve in a phosphorylation signaling pathway responding to salinity, and report potential cross-talk between the mosquito immune response and osmoregulation. This study provides a key step towards applying the growing molecular knowledge of these malaria vectors to improve understanding of their ecological tolerances and habitat occupancy.

The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles

“…Despite these parallel changes, a correlated evolution of both tolerances, constrained by identical genes and mechanisms (genetic correlation sensu Kellermann, Overgaard, Loeschcke, Kristensen, & Hoffmann, ;—i.e., our third hypothesis), is incompatible with the occurrence of species resistant to desiccation but with reduced hyporegulation ability, such as E. ochropterus . Nevertheless, further research identifying potential gene expression pathways related with either desiccation (e.g., Lopez‐Martinez et al., ) or salinity stress (e.g., Uyhelji, Cheng, & Besansky, ), as well as those common to both stressors, would be needed to shed light on the degree of mechanistic overlap between desiccation and salinity tolerances.…”

Complexities of gene expression patterns in natural populations of an extremophile fish (Poecilia mexicana, Poeciliidae)

“…Our results indicate that the choice of tissue substantially affects inferences about gene expression variation in nature. Many studies still focus on the analysis of single organs (Narum & Campbell, ; Wang et al., ), whole organisms (Gross et al., ) or lack formal analyses of how gene expression varies among organs (Hinaux et al., ; Uyhelji, Cheng, & Besansky, ). This is not necessarily problematic when a priori hypotheses are being tested, but a focus on single organs may also lead to skewed or misleading results that affect our inferences about organismal responses to environmental variation.…”

Cuticle hydrocarbons in saline aquatic beetles

“…Previous studies have reported differences in water loss rates between beetle species with different saline optima ( Pallarés et al, 2016 ) or between freshwater and saline populations of corixids ( Cannings, 1981 ), supporting such hypothesis. Furthermore, a recent transcriptomic study in Anopheles larvae has suggested that cuticle composition may be altered to deal with osmoregulatory stress by decreasing permeability in saline water, as cuticle and cytoskeleton genes were robustly induced at 40–50% seawater salinities ( Uyhelji, Cheng & Besansky, 2016 ).…”