Fatigue resistant jaw muscles facilitate long-lasting courtship behaviour in the southern alligator lizard (Elgaria multicarinata)

Abstract

The southern alligator lizard ( Elgaria multicarinata ) exhibits a courtship behaviour during which the male firmly grips the female's head in his jaws for many hours at a time. This extreme behaviour counters the conventional wisdom that reptilian muscle is incapable of powering high-endurance behaviours. We conducted in situ experiments in which the jaw-adductor muscles of lizards were stimulated directly while bite force was measured simultaneously. Fatigue tests were performed by stimulating the muscles with a series of tetanic trains. Our results show that a substantial sustained force gradually develops during the fatigue test. This sustained force persists after peak tetanic forces have declined to a fraction of their initial magnitude. The observed sustained force during in situ fatigue tests is consistent with the courtship behaviour of these lizards and probably reflects physiological specialization. The results of molecular analysis reveal that the jaw muscles contain masticatory and tonic myosin fibres. We propose that the presence of tonic fibres may explain the unusual sustained force properties during mate-holding behaviour. The characterization of muscle properties that facilitate extreme performance during specialized behaviours may reveal general mechanisms of muscle function, especially when done in light of convergently evolved systems exhibiting similar performance characteristics.

Sustained force production by the jaw‐adductor muscles of a megalophagous frog, Ceratophrys cranwelli

“…For the experiments, maximum activation of the jaw‐adductor muscles was desired. To determine the supramaximal voltage required to attain maximum contractile force from the muscle complex, established procedures used in similar muscle stimulation experiments were performed (Lappin et al, 2006; Clark & Peters 2006; Nguyen et al, 2020; Peters, 1994; Peters & Aulner, 2000). For this study, a series of tetanic contractions were induced with increasing voltage until supramaximal voltage could be determined (50–60 V, 60 Hz, 1000 mA, 0.1 ms pulses, 500 ms train).…”

“…Four frogs were used to quantify the force–frequency relationship of the jaw‐adductor complex to identify the stimulation frequency at which complete tetanic fusion occurs. This procedure was performed, following established methods used in similar experiments (Guelinckx et al, 1986; Kuffler & Williams, 1953; Lännergren, 1979; Lappin et al, 2006; Clark & Peters 2006; Nguyen et al, 2020; Peters & Aulner, 2000; Peters, 1994), by delivering 500 ms trains (80 V, 1000 mA, 0.1 ms pulses) at increasing frequencies (5, 10, 20, 30, 40, 50 Hz). The muscles were given 10 min of rest between each tetanus to mitigate the effects of fatigue.…”

“…With respect to jaw muscles, the courtship behavior of male southern alligator lizards ( Elgaria multicarinata ) provides an example of a high endurance behavior supported by sustained muscle force production. During courtship, the male continuously grips the head of the female with his jaws for up to 49 h (Nguyen et al, 2020; Pauly, 2019). When repeatedly stimulated in situ, the jaw‐adductor muscles of these lizards produce a significant sustained force between tetanic trains when the muscles are not being stimulated.…”

“…When repeatedly stimulated in situ, the jaw‐adductor muscles of these lizards produce a significant sustained force between tetanic trains when the muscles are not being stimulated. This sustained force remains even after peak tetanic forces greatly decline (Nguyen et al, 2020). The presence of a sustained force is evidence of potential specialization in the jaw muscles of these lizards.…”

Trade-offs in muscle physiology in selectively bred high runner mice

“…A subsequent twitch contraction was performed at optimum length. Peak twitch force was determined and time series data were used to calculate the time from onset of activation to peak twitch force (TP tw ), and the time from peak twitch force to 50% relaxation (TR 50 ) ( Marsh and Bennett, 1985 , 1986 ; Bennett et al, 1989 ; Askew and Marsh, 1997 ; Syme et al, 2005 ; Nguyen et al, 2020 ) ( Table 1 ).…”