Diversity in Morphology and Locomotory Behavior Is Associated with Niche Expansion in the Semi-aquatic Bugs

Abstract

SummaryAcquisition of new ecological opportunities is a major driver of adaptation and species diversification [1, 2, 3, 4]. However, how groups of organisms expand their habitat range is often unclear [3]. We study the Gerromorpha, a monophyletic group of heteropteran insects that occupy a large variety of water surface-associated niches, from small puddles to open oceans [5, 6]. Due to constraints related to fluid dynamics [7, 8, 9] and exposure to predation [5, 10], we hypothesize that selection will favor high speed of locomotion in the Gerromorpha that occupy water-air interface niches relative to the ancestral terrestrial life style. Through biomechanical assays and phylogenetic reconstruction, we show that only species that occupy water surface niches can generate high maximum speeds. Basally branching lineages with ancestral mode of locomotion, consisting of tripod gait, achieved increased speed on the water through increasing midleg length, stroke amplitude, and stroke frequency. Derived lineages evolved rowing as a novel mode of locomotion through simultaneous sculling motion almost exclusively of the midlegs. We demonstrate that this change in locomotory behavior significantly reduced the requirement for high stroke frequency and energy expenditure. Furthermore, we show how the evolution of rowing, by reducing stroke frequency, may have eliminated the constraint on body size, which may explain the evolution of larger Gerromorpha. This correlation between the diversity in locomotion behaviors and niche specialization suggests that changes in morphology and behavior may facilitate the invasion and diversification in novel environments.

Escalation and constraints of antagonistic armaments in water striders

“…Sequences were retrieved from in house transcriptome databases and from (39) for the following markers: 12S RNA; 16S RNA; 18S RNA; 28S RNA; Cytochrome Oxydase subunit I (COI); Cytochrome Oxydase subunit II (COII); Cytochrome Oxydase subunit III (COIII); Cytochrome b (cyt b); NADH-ubiquinone oxidoreductase chain 1 (ND1); Ultrabithorax (Ubx); Sex combs reduced (Scr); Gamma interferon inducible thiol reductase (gilt); Antennapedia (Antp); Distal-less (dll); Doublesex (dsx) . All these markers were submitted to GenBank and their accession numbers can be found in the Dryad Digital Repository: Will be provided before publication (or upon request) .…”

“…All these markers were submitted to GenBank and their accession numbers can be found in the Dryad Digital Repository: Will be provided before publication (or upon request) . Phylogenetic reconstruction (Figure S5) was performed using MrBayes version 3.2.6 and PhyML version 3.0 in Geneious 7.1.9 as described in (39). Concatenation of sequence alignments and phylogenetic tree in Newick format are also available in the Dryad Digital Repository: Will be provided before publication (or upon request) .…”

The genome of the water striderGerris buenoireveals expansions of gene repertoires associated with adaptations to life on the water

“…The invasion of this new habitat provided access to resources previously underutilized by insects and made the Gerromorpha the dominant group of insects at water surfaces. This novel specialized life style makes the Gerromorpha an exquisite model system to study how new ecological opportunities can drive adaptation and species diversification 2,9-11 .…”

“…The shift in habitat exposed these insects to new selective pressures that are divergent from their terrestrial ancestors. The Gerromorpha face two primary challenges unique among insects: how to remain afloat and how to generate efficient thrust on the fluid substrate 2,3,12 . The bristles covering the legs of water striders, owing to their specific arrangement and density, act as a non-wetting structures capable of exploiting water surface tension by trapping air between the leg and water surface and keeping them afloat (Figure 1A) 2,3,12,13 .…”

“…The Gerromorpha face two primary challenges unique among insects: how to remain afloat and how to generate efficient thrust on the fluid substrate 2,3,12 . The bristles covering the legs of water striders, owing to their specific arrangement and density, act as a non-wetting structures capable of exploiting water surface tension by trapping air between the leg and water surface and keeping them afloat (Figure 1A) 2,3,12,13 . Locomotion, on the other hand, is made possible through changes in the morphology and the patterns of leg movement (Figure 1B) 2,3,12,13 Two modes of locomotion are employed: an ancestral mode using the tripod gait through alternating leg movements, and a derived mode using the rowing gait through simultaneous sculling motion of the pair of middle legs (Figure 1B) 2,12 .…”