Parallel and divergent morphological adaptations underlying the evolution of jumping ability in ants

Jumping is a rapid locomotory mode widespread in terrestrial organisms.
However, it is a rare specialization in ants. Forward jumping has been
reported within four distantly related ant
genera: Gigantiops, Harpegnathos, Myrmecia, and
Odontomachus. The temporal engagement of legs/body parts during jump,
however, varies across these genera. It is unknown what morphological
adaptations underlie such behaviors and whether jumping in ants is solely
driven directly by muscle contraction or additionally relies on elastic
recoil mechanism. We investigate the morphological adaptations for jumping
behavior by comparing differences in the locomotory musculature between
jumping and non-jumping relatives using X-ray micro-CT and 3D
morphometrics. We found that the size-specific volumes of the trochanter
depressor muscle (scm6) of the middle and hind legs are 3–5 times larger
in jumping ants, and that one coxal remotor muscle (scm2) is reduced in
volume in the middle and/or hind legs. Notably, the enlargement in the
volume of other muscle groups is directly linked to the legs or body parts
engaged during the jump. Furthermore, a direct comparison of the muscle
architecture revealed two significant differences between jumping versus
non-jumping ants: First, the relative Physiological Cross-Sectional Area
(PCSA) of the trochanter depressor muscles of all three legs was larger in
jumping ants, except in the front legs of O. rixosus and M. nigrocincta;
second, the relative muscle fiber length was shorter in jumping ants
compared to non-jumping counterparts, except in the front legs of O.
rixosus and M. nigrocincta. This suggests that the difference in relative
muscle volume in jumping ants is largely invested in the area (PCSA), and
not in fiber length. There was no clear difference in the pennation angle
between jumping and non-jumping ants. However, the hind leg length
relative to body length was longer in jumping ants. Based on direct
comparison of the observed vs. possible work and power output during
jumps, we surmise that direct muscle contractions suffice to explain
jumping performance, in two species, but elastic recoil is likely
important in one. We suggest that increased investment in jumping-relevant
musculature is a primary morphological adaptation that separates jumping
from non-jumping ants. These results elucidate the common and
idiosyncratic morphological changes underlying this rare adaptation in
ants.