The influence of feeding on the evolution of sensory signals: a comparative test of an evolutionary trade‐off between masticatory and sensory functions of skulls in southern African Horseshoe bats (Rhinolophidae)

Abstract

The skulls of animals have to perform many functions. Optimization for one function may mean another function is less optimized, resulting in evolutionary trade-offs. Here, we investigate whether a trade-off exists between the masticatory and sensory functions of animal skulls using echolocating bats as model species. Several species of rhinolophid bats deviate from the allometric relationship between body size and echolocation frequency. Such deviation may be the result of selection for increased bite force, resulting in a decrease in snout length which could in turn lead to higher echolocation frequencies. If so, there should be a positive relationship between bite force and echolocation frequency. We investigated this relationship in several species of southern African rhinolophids using phylogenetically informed analyses of the allometry of their bite force and echolocation frequency and of the three-dimensional shape of their skulls. As predicted, echolocation frequency was positively correlated with bite force, suggesting that its evolution is influenced by a trade-off between the masticatory and sensory functions of the skull. In support of this, variation in skull shape was explained by both echolocation frequency (80%) and bite force (20%). Furthermore, it appears that selection has acted on the nasal capsules, which have a frequency-specific impedance matching function during vocalization. There was a negative correlation between echolocation frequency and capsule volume across species. Optimization of the masticatory function of the skull may have been achieved through changes in the shape of the mandible and associated musculature, elements not considered in this study.

Go big or go fish: morphological specializations in carnivorous bats

“…Interestingly, all extant species of carnivorous and animalivorous bats emit echolocation calls nasally, whereas most insectivorous and both piscivorous bat species are oral echolocators. Recent work on a family of nasal echolocating bats (Rhinolophidae) demonstrated trade-offs between masticatory and sensory functions; higher bite forces, a product of a shorter rostrum, are associated with higher echolocation frequencies [76]. Simultaneously, resting frequency and pulse repetition scale negatively with bat size, and pulse duration scales positively with body mass in certain species [77,78].…”

The relative contribution of drift and selection to phenotypic divergence: A test case using the horseshoe bats Rhinolophus simulator and Rhinolophus swinnyi

“…These adaptive complexes can also include skull shape and size because it houses features for the production and reception of sensory signals while also functioning in handling and mastication of food. This has been evident in both mammals and birds (Freeman & Lemen, 2010;Jacobs, Bastian, & Bam, 2014). Nevertheless, several studies have also implicated drift in the evolution of acoustic signals that are used in reproduction rather than orientation, for example, in Neotropical singing mice (Campbell et al, 2010), anurans (Ohmer, Robertson, & Zamudio, 2009), and in birds (Irwin, Thimgan, & Irwin, 2008).…”

The allometry of echolocation call frequencies in horseshoe bats: nasal capsule and pinna size are the better predictors than forearm length

“…RF of R. clivosus s.l. is almost 40 kHz above that expected based on body mass), which may be because selection increase bite force and then promote a decrease in snout length, and thus could in turn lead to higher frequencies (Jacobs et al ., ). Santana & Lofgren () showed that horseshoe bats in Africa and Mediterranean regions have a proportionally taller skull and a narrower rostrum with a smaller nasal capsule, which may explain partly that several species emit frequencies that are higher than what would be expected based on body size.…”

“…The nasal capsules enhance the second harmonic of the echolocation calls by forming part of a frequency-specific impedance matching system during vocalization (Hartley & Suthers, 1988;Pedersen, 1998). Differences in size and shape of the nasal capsules have been found across horseshoe bat species, and have been seen as a cause behind divergences in echolocation frequency among populations within a species (Armstrong & Coles, 2007;Odendaal & Jacobs, 2011) as well as across species (Jacobs et al, 2014). Here, we found that RF was significantly and negatively related to both NSH and PC1 extracted from the measurements of the nasal capsules among horseshoe bats.…”

“…Recently, Jacobs et al . () reported that echolocation frequency is negatively correlated with nasal capsule volume among 10 species of rhinolophids. Therefore, the studies indicated that the nasal capsule of horseshoe bats may provide preferably a functional explanation relative to their peak frequency that may be preferable to FA.…”