Overcoming mechanical adversity in extreme hindleg weapons

Abstract

The size of sexually selected weapons and their performance in battle are both critical to reproductive success, yet these traits are often in opposition. Bigger weapons make better signals. However, due to the mechanical properties of weapons as lever systems, increases in size may inhibit other metrics of performance as different components of the weapon grow out of proportion with one another. Here, using direct force measurements, we investigated the relationship between weapon size and weapon force production in two hindleg weapon systems, frog-legged beetles (Sagra femorata) and leaf-footed cactus bugs (Narnia femorata), to test for performance tradeoffs associated with increased weapon size. In male frog-legged beetles, relative force production decreased as weapon size increased. Yet, absolute force production was maintained across weapon sizes. Surprisingly, mechanical advantage was constant across weapon sizes and large weaponed males had disproportionately large leg muscles. In male leaf-footed cactus bugs, on the other hand, there was no relationship between weapon size and force production, likely reflecting the importance of their hindlegs as signals rather than force-producing structures of male-male competition. Overall, our results suggest that when weapon force production is important for reproductive success, large weaponed animals may overcome mechanical challenges by maintaining proportional lever components and investing in (potentially costly) compensatory mechanisms.

Fig 1

A) Mating S. femorata (male on top, photo: D. O’Brien). B) Male N. femorata (photo: R. Boisseau). C-E) Illustrations of lever systems. C) S. femorata hindlimb. D) Simplified machine. E) N. femorata hindlimb. Components of lever systems color coded across all structures (L_in = input lever (brown), L_out = output lever (dark blue), F_in = force in (orange), F_out = force out (light blue), fulcrum (light red)). All are best described as 3^rd order levers.

Fig 2. Interaction outcome and escalation in S. femorata.

A) Interaction outcome. Red line represents logistical regression of interaction outcome (Male A or B wins) in relation to the difference in competitor weapon size (Femur length; FL_A − FL_B). Positive x values indicate Male A had a larger weapon size than the opponent. Negative x values indicate that Male B had a larger weapon size than the opponent. B) Interaction escalation. Red line represents generalized linear model between interaction escalation level and absolute difference in weapon size (Femur length; |FL_A − FL_B|).

Fig 3. Relationship between maximum squeezing force and weapon size for A) male S. femorata, B) male N. femorata, C) female S. femorata, and D) female N. femorata.

Red lines represent OLS regression. Shaded areas represent 95% confidence intervals around OLS regressions. Lines omitted for non-significant regressions.

Fig 4. Relationship between weapon size and body size for A) male S. femorata, B) male N. femorata, C) female S. femorata, and D) female N. femorata.

Red lines represent OLS regression. Shaded areas represent 95% confidence intervals around OLS regressions.

Fig 5. Relationships between lever components/mechanical advantage and body size for A) S. femorata males, B) S. femorata females, C) N. femorata males, and D) N. femorata females.

Top: L_in vs. body size. Middle: L_out vs. body size. Bottom: mechanical advantage vs. body size. Red lines represent OLS regression. Shaded areas represent 95% confidence intervals around OLS regressions. Lines omitted for non-significant regressions.

Fig 6. Relationship between hindlimb muscle mass and body size for A) male S. femorata, B) male N. femorata, C) female S. femorata, and D) female N. femorata.

Red lines represent OLS regression. Shaded areas represent 95% confidence intervals around OLS regressions.