Seismic communication in a blind subterranean mammal: a major somatosensory mechanism in adaptive evolution underground.

Abstract

Seismic communication, through lowfrequency and patterned substrate-borne vibrations that are generated by head thumping, and which travel long distances underground, is important in the nonvisual communication of subterranean mole rats of the Spalax ehrenbergi superspecies (2n = 52, 54, 58, and 60) in Israel. This importance pertains both intraspecifically in adaptation and interspecifically in speciation. Neurophysiologic, behavioral, and anatomic findings in this study suggest that the mechanism of long-distance seismic communication is basically somatosensory and is independent of the auditory mechanism. Seismic communication thus appears to be a channel ofcommunication important in the evolution of subterranean mammals that display major adaptation to life underground.What happens evolutionarily when a major sense organ atrophies and therefore a major communication mode, such as vision, is eliminated? Will other sense organs and communication channels compensate (1, 2)? We have extensively studied this problem in blind (3) subterranean mole rats of the Spalax ehrenbergi superspecies in Israel. The superspecies consists of four, parapatrically distributed, young sibling chromosomal species (2n = 52, 54, 58, and 60). Each species is adapted at multiple molecular and organismal levels to underground life and to four increasingly arid climates (4-7). Regressive evolution of the atrophied eye (8-10) in S. ehrenbergi was coupled with progressive evolution in photoperiod perception (11) and biorhythmicity (12). Olfactory communication (13) is also an important ethological reproductive isolating mechanism underlying assortative mating and enhancing speciation. Progressive evolution of short-range acoustic communication in S. ehrenbergi was described behaviorally (14), physically (15), transmissionally (16), and morphophysiologically (17,18 (19,21). Underground seismic communication is therefore important in adaptation within populations and in speciation between diverging mole rat populations.Although the inter-individual and species-specific behavioral patterns of seismic signaling are known (19-21), the perceptive mechanism and neuronal processing of this communication modality remain obscure in subterranean mammals (23) and generally so in all animals (24). Fay and Popper (25) speculated that substrate-borne vibrations are mediated by bone conduction through massive auditory ossicles analogous in function to the otoliths of fish, by providing an inertial mechanism of detection of relative skull movement. Rado et al. (26) suggested that in mole rats the transmission of vibrational signals is mediated by contact of the mandible with the tympanic bulla through the ear to the brain, compensating for the limitation in receiving air-borne signals.Here we demonstrate that in mole rats of the S. ehrenbergi superspecies the mechanism of seismic signaling through substrate-borne vibrations is basically somatosensory and functions independently of the auditory mechanism. We suggest that in mole rats, and apparen...

Exploration and navigation in the blind mole rat (Spalax ehrenbergi): global calibration as a primer of spatial representation

“…Although mole rats' eyes had undergone degeneration during the course of their evolution, the mole rats have evolved effective compensatory means to efficiently navigate and find their way. Indeed, mole rats were found to have strong tactile Klauer et al, 1997) and magnetic sensory abilities Kimchi and Terkel, 2001a), and produce and utilize seismic vibrations (Kimchi et al, 2005;Nevo et al, 1991), all of which could facilitate the mapping of an unfamiliar environment. Most importantly, the mole rat seems to have developed a spatial representation capacity that is comparable with that of sighted rodents, and in some cases may even exceed them; e.g.…”

Mammalian evolution underground. The ecological-genetic-phenetic interfaces

“…Mole rats communicate vibrational^ during agonistic encounters and respond to played-back stimuli . Field observations (Nevo et al 1991a) and experiments (Z. Katzir and E. Nevo, in prep.) suggest inter-territorial communication.…”

“…Seismic, nonvisual communication in mole rats Spalax provides a major somatosensory mechanism in adaptive evolution underground, both in adaptation and speciation , Rado et al 1987, Nevo et al 1991a. The brain mapping of the cortex of Spalax ehrenbergi was explored for somatosensory responses with special reference to an extension into the occipital cortex which serves vision in sighted mammals (Necker et al 1992).…”

“…Vibrational, seismic communication has been extensively described in Spalax , 1991, Rado et al 1987, Nevo et al 1991a. The seismic signals are produced by thumping of the flat head (which originally serves to bulldoze soil and compact the tunnel) against the tunnel ceiling.…”

“…Seismic communication also appears to act as premating isolating mechanism in speciation , 1991, Nevo et al 1991a. Thus, underground seismic communication is important in adaptation within populations, in interindividual communication between territories, and in speciation between diverging mole rat populations.…”