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The physiological adaptation for the “fore-mid” four-legged walking behavior of the pygmy mole cricket Xya sichuanensis

Yi Zhang, Shuying Wang, Zhu-Jun Feng, Tong-Xian Liu, Chengquan Cao

Preprint posted on 2 April 2020 https://www.biorxiv.org/content/10.1101/2020.03.22.002675v2

The floor is lava for pygmy mole cricket hind legs: X. sichuanensis walks and runs only on its fore and mid legs, while conserving hind legs for jumping. These are flexed + held in grooves along the abdomen forming a specialized structure

Selected by Matt Muzzatti

Background

Pygmy mole crickets (Orthoptera: Tridactylidae) are an incredible product of natural selection; they have unique mole-like forelegs used for building burrows, and like many other Orthoptera species have well-developed hind legs used for jumping. Some Tridactylidae can even launch themselves off the surface of water using highly specialized hind legs (Burrows and Picker 2010; Burrows and Sutton 2012). But this specialization is not without a trade-off, as Xya sichuanensis, a pygmy mole cricket native to Leshan, China, has been observed walking only on its fore and mid legs. Quadrupedalism (four-legged walking) has been recorded in other insects such as mantids, water striders, and brush-footed butterflies, but these insects have modified forelegs used for seizing prey and walk on their mid and hind legs. Although most Orthoptera have specialized hopping hind legs, they use a tripedal strut using all six legs. In this preprint, Zhang et al. used scanning electron microscopy, histological staining, and walking pattern analysis to analyze the “fore-mid leg” walking motion of X. sichuanensis and its associated morphological adaptations.

Figure 1. Dorsal (A) and transverse (B) views of Xya sichuanensis. From Zhang et al. 2020 under a CC-BY-NC-ND 4.0 International license.

Key findings

It was confirmed that the hind legs do not contact the ground when stationary, walking, or running, which is accomplished by ‘flexing’ the hind legs (tibia is resting on top of the femur, Fig. 2C). This walking style is assisted by a comparatively wider supporting area for four legs, relative to other insects. The flexed hind legs fit into grooves along the dorsal surface of the abdomen, and combined with short wings, fit together to form an integrated structure (Fig. 2E). The ventral abdominal cuticle remains in contact with the ground acting as a fulcrum point and is significantly thicker than other abdominal cuticles. This thickened abdomen is hypothesized to protect the cricket from friction while walking or running.

Two different movement patterns were discovered, one for walking and another for running, which allow for the specialized four-legged movement in X. sichuanensis.

Zhang et al. argue that the highly specialized hind legs of X. sichuanensis indicate that natural selection favoured improved jumping over six-legged walking, and thus during its evolutionary pathway, jumping was more important for its survival. This in turn drove the other four legs and the abdomen to evolve in support of walking.

Figure 2. A sketch of Xya sichuanensis hing leg (C) and the hind leg-wing-abdomen process (E). From Zhang et al. 2020 under a CC-BY-NC-ND 4.0 International license.

What I like about this preprint

I focused on the incredible morphology displayed in these crickets – the hing leg-wing-abdomen process is a beautiful product of evolution, and is eloquently illustrated by the authors. It reminds me of a transformer toy from childhood, where many different pieces fit together perfectly in a picturesque model of design and engineering. This preprint includes some fantastic in-depth diagrams of the slow-walking and running patterns exhibited by X. sichuanensis, so if behaviour is your thing, I highly suggest reading this paper.

The figures and diagrams in this manuscript are gorgeous. I only included a few figures from the manuscript, but the scanning electron micrographs and histological abdomen cross section figures are worth checking out.

Finally, this is a wonderful depiction of a highly specialized morphological adaptation resulting in a unique insect behaviour. This study contributes to the already weird and wonderful world of insects and provides valuable insight into movement behaviour among insects.

Future directions

Some open questions Zhang et al. propose include:

  • How does the jumping behaviour of X. sichuanensis drive organ specialization?
  • How does X. sichuanensis adapt to complex walking conditions?

Question for the authors

If adult crickets were used in this experiment, could the thickened cuticle on the abdomen just be a result of a lifetime of friction, sort of how callouses develop on human skin? Or are X. sichuanensis born with thickened cuticles and maintain that feature through its nymphal stages?

References

Burrows, M. and Picker, M.D. 2010. Jumping mechanisms and performance of pygmy mole crickets (Orthoptera, Tridactylidae). Journal of Experimental Biology 213, 2386-2398.

Burrows, M. and Sutton, G.P. 2012. Pygmy mole crickets jump from water. Current Biology 22, R990-R991.

Zhang, Y., Wang, S., Feng, Z.J., Lie, T.X., and Cao, C. 2020. The physiological adaptation for the “fore-mid” four-legged walking behavior of the pygmy mole cricket Xya sichuanensis. Preprint posted April 2, 2020. https://doi.org/10.1101/2020.03.22.002675

 

Posted on: 25 April 2020 , updated on: 11 May 2020

doi: https://doi.org/10.1242/prelights.19335

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