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Flight loss linked to faster molecular evolution in insects.

ABSTRACT: The loss of flight ability has occurred thousands of times independently during insect evolution. Flight loss may be linked to higher molecular evolutionary rates because of reductions in effective population sizes (Ne) and relaxed selective constraints. Reduced dispersal ability increases population subdivision, may decrease geographical range size and increases (sub)population extinction risk, thus leading to an expected reduction in Ne. Additionally, flight loss in birds has been linked to higher molecular rates of energy-related genes, probably owing to relaxed selective constraints on energy metabolism. We tested for an association between insect flight loss and molecular rates through comparative analysis in 49 phylogenetically independent transitions spanning multiple taxa, including moths, flies, beetles, mayflies, stick insects, stoneflies, scorpionflies and caddisflies, using available nuclear and mitochondrial protein-coding DNA sequences. We estimated the rate of molecular evolution of flightless (FL) and related flight-capable lineages by ratios of non-synonymous-to-synonymous substitutions (dN/dS) and overall substitution rates (OSRs). Across multiple instances of flight loss, we show a significant pattern of higher dN/dS ratios and OSRs in FL lineages in mitochondrial but not nuclear genes. These patterns may be explained by relaxed selective constraints in FL ectotherms relating to energy metabolism, possibly in combination with reduced Ne.

SUBMITTER: Mitterboeck TF

PROVIDER: S-EPMC3735250 | biostudies-literature | 2013 Sep

REPOSITORIES: biostudies-literature

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Flight loss linked to faster molecular evolution in insects.

Mitterboeck T Fatima TF Adamowicz Sarah J SJ

Proceedings. Biological sciences 20130724 1767

The loss of flight ability has occurred thousands of times independently during insect evolution. Flight loss may be linked to higher molecular evolutionary rates because of reductions in effective population sizes (Ne) and relaxed selective constraints. Reduced dispersal ability increases population subdivision, may decrease geographical range size and increases (sub)population extinction risk, thus leading to an expected reduction in Ne. Additionally, flight loss in birds has been linked to hi ...[more]

PMID: 23884090

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Project description:Ultraspiracle protein/retinoid X receptor (USP/RXR) is a nuclear receptor and transcription factor which is an essential component of a heterodimeric receptor complex with the ecdysone receptor (EcR). In insects this complex binds ecdysteroids and plays an important role in the regulation of growth, development, metamorphosis and reproduction. In some holometabolous insects, including Lepidoptera and Diptera, USP/RXR is thought to have experienced several important shifts in function. These include the acquisition of novel ligand-binding properties and an expanded dimerization interface with EcR. In light of these recent hypotheses, we implemented codon-based likelihood methods to investigate if the proposed shifts in function are reflected in changes in site-specific evolutionary rates across functional and structural motifs in insect USP/RXR sequences, and if there is any evidence for positive selection at functionally important sites. Our results reveal evidence of positive selection acting on sites within the loop connecting helices H1 and H3, the ligand-binding pocket, and the dimer interface in the holometabolous lineage leading to the Lepidoptera/Diptera/Trichoptera. Similar analyses conducted using EcR sequences did not indicate positive selection. However, analyses allowing for variation across sites demonstrated elevated non-synonymous/synonymous rate ratios (d(N)/d(S)), suggesting relaxed constraint, within the dimerization interface of both USP/RXR and EcR as well as within the coactivator binding groove and helix H12 of USP/RXR. Since the above methods are based on the assumption that d(S) is constant among sites, we also used more recent models which relax this assumption and obtained results consistent with traditional random-sites models. Overall our findings support the evolution of novel function in USP/RXR of more derived holometabolous insects, and are consistent with shifts in structure and function which may have increased USP/RXR reliance on EcR for cofactor recruitment. Moreover, these findings raise important questions regarding hypotheses which suggest the independent activation of USP/RXR by its own ligand.

Project description:Recent debates on insect decline require sound assessments on the relative drivers that may negatively impact insect populations. Often, baseline data rely on insect monitorings that integrate catches over long time periods. If, however, effects of time-critical environmental factors (e.g., light pollution) are of interest, higher temporal resolution of insect data is required during very specific time intervals (e.g., between dusk and dawn). Conventional time-critical insect trapping is labour-intensive (manual activation/deactivation) and temporally inaccurate as not all traps can be serviced synchronically at different sites. Also, temporal shifts of environmental conditions (e.g., sunset/sunrise) are not accounted for. We present a battery-driven automated insect flight-interception trap which samples insects during seven user-defined time intervals. A commercially available flight-interception trap is fitted to a turntable containing eight positions, seven of them holding cups and one consisting of a pass-through hole. While the cups sample insects during period of interest, the pass-through hole avoids unwanted sampling during time-intervals not of interest. Comparisons between two manual and two automated traps during 71 nights in 2018 showed no difference in caught insects. A study using 20 automated traps during 104 nights in 2019 proved that the automated flight-interception traps are reliable. The automated trap opens new research and application possibilities as arbitrary insect-sampling intervals can be defined. The trap proves efficient, saving manpower and associated costs as activation/deactivation is required only every seven sampling intervals. In addition, the timing of the traps is accurate, as all traps sample at exactly the same intervals and ensure comparability. The automated trap is low maintenance and robust due to straightforward technical design. It can be controlled manually or via smartphone through a Bluetooth connection. Full construction details are given in Appendices.

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Flight loss linked to faster molecular evolution in insects.

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Flight loss linked to faster molecular evolution in insects.

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