Abstract
BackgroundHow adaptive phenotypes are shaped by the action of key developmental genes during ontogeny remains poorly understood. Water striders, a group of hemipteran insects, present a unique example of adaptation to life on the fluid water surface substrate. The group has undergone a set of leg modifications allowing them to efficiently move on the water surface and hence invade a variety of niches from ponds to open oceans. The elongated legs of water striders play a key role in generating efficient movement on the fluid by acting as propelling oars.ResultsTo determine the developmental mechanisms underlying leg elongation, we examined the function of the key developmental genes decapentaplegic (dpp), wingless (wg), epidermal growth factor receptor (egfr), and hedgehog (hh) during embryonic development in the water strider Limnoporus dissortis. By analyzing expression patterns and RNAi knockdown phenotypes, we uncover the role of these genes in leg growth and patterning during embryogenesis. Our results indicate that wg and egfr contribute to the elongation of all the three segments of all thoracic legs, whereas hh specifies distal leg segments.ConclusionsTogether, our results suggest that key patterning genes contribute to the dramatic elongation of thoracic appendages in water striders.
Highlights
How adaptive phenotypes are shaped by the action of key developmental genes during ontogeny remains poorly understood
Affected embryos show truncation of distal leg segments. (E) Moderate hh ribonucleic acid interference (RNAi) embryos showing patterning defects. (F) Segmentation defects aggravate in severe hh RNAi where only the head and the first thoracic segment could be distinguished, and all the legs are distally truncated. (G) Measurement of mild hh RNAi legs showing increased length of the femur in all three legs
An asterisk indicates that the test was significant at (P ≤ 0.01). hh: hedgehog; RNAi: gene knockdown using ribonucleic acid interference; T1, 2, 3: thoracic segments 1, 2, 3; WT: wild type
Summary
How adaptive phenotypes are shaped by the action of key developmental genes during ontogeny remains poorly understood. Water striders belong to a monophyletic group of semiaquatic heteropteran insects, known as semiaquatic bugs, which represent a remarkable example of adaptation to water surface life, enabling them to invade various aquatic niches including open oceans [2]. Semiaquatic bugs follow a hemimetabolous mode of development where embryos hatch in a nymphal form which will undergo five successive molts to reach the mature adult stage [2]. In many water striders including Limnoporus dissortis, Ubx is expressed in both mid- and rear legs and functions to elongate the mid-legs but to shorten the rear legs [3,4,5]. These opposing functions of Ubx are achieved through the emergence of sensitivity of leg tissues to differences in Ubx dose, thereby establishing the relative differences
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