Patterns of praying mantis auditory system evolution based on morphological, molecular, neurophysiological, and behavioural data

Abstract

Some praying mantids have sensitive ultrasonic hearing arising from a unique 'cyclopean' ear located in the ventral metathorax. The present study explores the evolutionary history of the mantis auditory system by integrating large anatomical, neurophysiological, behavioural, and molecular databases. Using an 'auditory phylogeny' based on 13 morphological characters, we identified a primitively earless form of metathoracic anatomy in several extant taxa. In addition, there are five distinct mantis auditory systems. Three of these can be identified anatomically, and the other two can only be detected neurophysiologically. Superimposing these results onto a phylogenetic tree derived from molecular data from seven genes shows that the cyclopean mantis ear evolved once approximately 120 Mya. All the other auditory system types are either varying degrees of secondary loss, or are recent innovations that each occurred independently multiple times. The neurophysiological response to ultrasound is remarkably consistent across all taxa tested, as is the multicomponent, in-flight behaviour triggered by ultrasound. Thus, mantids have an ancient, highly conserved auditory neural-behavioural system. Although ultrasonic hearing in several insect groups evolved in response to bat predation, mantis hearing predates the appearance of bats (approximately 63 Mya) and must originally have functioned in communication, prey detection, or avoidance of nonbat predators.

The phylogenetic system of Mantodea (Insecta: Dictyoptera)

“…This is supported by the presence of a setigerous tubercle in the position of the tibial spur in extant Chaeteessa (Roy 1999: 38) (see character 68, discussion in . The position of Chaeteessa as the sistergroup of the remaining Mantodea was not supported in the analysis by Yager & Svenson (2008: fig. 6) but was found in the molecular analysis by Svenson & Whiting (2009: fig.…”

“…The assumed monophyly of Mantodea is well supported by morphological characters (Hennig 1969(Hennig , 1981Ax 1999;Klass 1995Klass , 1997Deitz et al 2003;Klass & Meier 2006;Klass & Eulitz 2007;Ware et al 2008;Klass et al 2009) and molecular data (Svenson & Whiting 2003, 2004aTerry & Whiting 2005;Kjer et al 2006;Inward et al 2007;Lo et al 2007;Fenn et al 2008;Ware et al 2008;Yager & Svenson 2008). Klass & Ehrmann (2003: 196) listed the following autapomorphies for Mantodea.…”

“…7.60). Roy (1999: 37) Morphological and several molecular datasets have repeatedly found Mantoida to be the sistergroup of the remaining extant Mantodea (Klass 1995(Klass , 1997Svenson & Whiting 2004a;Klass & Meier 2006;Inward et al 2007;Lo et al 2007;Ware et al 2008;Yager & Svenson 2008). Jantsch (1999) found a basal split between a monophyletic Mantoida + Chaeteessa and the remaining (predominantly Neotropical) Mantodea in his morphological analysis.…”

“…This will also include those structures that have been assumed by previous authors to have evolved convergently. The results are compared with the most comprehensive genetic analyses (mainly Svenson & Whiting 2009, but also Whiting 2004a andSvenson 2008), and with the typological classification by Ehrmann (2002).…”

Variability in Sensory Ecology: Expanding the Bridge Between Physiology and Evolutionary Biology

“…However, our knowledge about how sensory systems have diverged in both form and functional properties at the species level remains fragmentary and, to date, is limited to a handful of studies that have investigated relationships between the evolutionary development of species and the efficiency of their communication signals (e.g., Parker et al 1998;Prum and Torres 2003;Smith et al 2004;Wickham et al 2006;Cummings 2007;Douglas et al 2007;Briscoe 2008;Lavoué et al 2008;Yager and Svenson 2008). Some of these studies have used phylogenetic methods to infer the ancestral sensory conditions of extant species and have then tested whether evolution has occurred in the predicted direction upon invasion of new habitats.…”