Receiver bias and the acoustic ecology of aye-ayes (Daubentonia madagascariensis)

Abstract

The aye-aye is a rare lemur from Madagascar that uses its highly specialized middle digit for percussive foraging. This acoustic behavior, also termed tap-scanning, produces dominant frequencies between 6 and 15 kHz. An enhanced auditory sensitivity to these frequencies raises the possibility that the acoustic and auditory specializations of aye-ayes have imposed constraints on the evolution of their vocal signals, especially their primary long-distance vocalization, the screech. Here we explore this concept, termed receiver bias, and suggest that the dominant frequency of the screech call (~2.7 kHz) represents an evolutionary compromise between the opposing adaptive advantages of long-distance sound propagation and enhanced detection by conspecific receivers.

Do aye-ayes echolocate? Studying convergent genomic evolution in a primate auditory specialist

“…Specifically, we observed unexpectedly significant enrichments for convergent amino acids between echolocating bats and mouse and elephant. Interestingly, mice have been observed to communicate in the ultrasound during courtship and mating (Musolf et al 2010), with a frequency comparable to that 365 used by many echolocating bats (~70 kHz; White et al 1998), and outside the range of aye-aye auditory ability (Ramsier and Dominy 2012). Perhaps the observed convergent evolution between mouse and echolocating bats at these loci is spurred by the demands of high-ultrasound processing rather than echolocation behavior?…”

“…Among other unique adaptations, ayeayes possess an elongated and highly flexible middle finger with which they tap rapidly along the surface of trees in the search for the internal mines of wood-boring insect larvae (Erickson 60 1991;Sterling and Povinelli 1999;Schwitzer et al 2013; Thompson et al 2016). The resulting differential soundings of a tree's variable interior structures are received by aye-ayes' large, alert, high-frequency attuned pinna (Coleman and Ross, 2004;Ramsier and Dominy, 2012) and processed by a relatively enlarged inferior colliculus in a brain that is also overall the largest relative to body size among all extant strepsirrhine primates (Smith and Jungers 1997;Kaufman 65 et al 2005). In addition to acoustic signals, tactile and olfactory cues are also hypothesized to play important roles in aye-aye foraging ecology (Erickson, 1991;Bush and Allman, 2004;Kaufman et al, 2005;Ramsier and Dominy, 2012).…”

“…The resulting differential soundings of a tree's variable interior structures are received by aye-ayes' large, alert, high-frequency attuned pinna (Coleman and Ross, 2004;Ramsier and Dominy, 2012) and processed by a relatively enlarged inferior colliculus in a brain that is also overall the largest relative to body size among all extant strepsirrhine primates (Smith and Jungers 1997;Kaufman 65 et al 2005). In addition to acoustic signals, tactile and olfactory cues are also hypothesized to play important roles in aye-aye foraging ecology (Erickson, 1991;Bush and Allman, 2004;Kaufman et al, 2005;Ramsier and Dominy, 2012). Once a suitable location on the deadwood is detected, the aye-aye uses its large, continuously-growing incisors to gnaw through the tree's exterior and extract the larvae within using the flexible middle finger (Erickson, 1991;Soligo, 70 2005).…”

Testing Convergent Evolution in Auditory Processing Genes between Echolocating Mammals and the Aye-Aye, a Percussive-Foraging Primate

“…Among other unique adaptations, aye-ayes possess an elongated and highly flexible middle finger with which they tap rapidly along the surface of trees in the search for the internal mines of wood-boring insect larvae ( Erickson 1991 ; Sterling and Povinelli 1999 ; Schwitzer et al 2013 ; Thompson et al 2016 ). The resulting differential soundings of a tree’s variable interior structures are received by aye-ayes’ large, alert, high-frequency attuned pinna ( Coleman and Ross 2004 ; Ramsier and Dominy 2012 ) and processed by a relatively enlarged inferior colliculus in a brain that is also overall the largest relative to body size among all extant strepsirrhine primates ( Smith and Jungers 1997 ; Kaufman et al 2005 ). In addition to acoustic signals, tactile and olfactory cues are also hypothesized to play important roles in aye-aye foraging ecology ( Erickson 1991 ; Bush and Allman 2004 ; Kaufman et al 2005 ; Ramsier and Dominy 2012 ).…”

“…The resulting differential soundings of a tree’s variable interior structures are received by aye-ayes’ large, alert, high-frequency attuned pinna ( Coleman and Ross 2004 ; Ramsier and Dominy 2012 ) and processed by a relatively enlarged inferior colliculus in a brain that is also overall the largest relative to body size among all extant strepsirrhine primates ( Smith and Jungers 1997 ; Kaufman et al 2005 ). In addition to acoustic signals, tactile and olfactory cues are also hypothesized to play important roles in aye-aye foraging ecology ( Erickson 1991 ; Bush and Allman 2004 ; Kaufman et al 2005 ; Ramsier and Dominy 2012 ). Once a suitable location on the deadwood is detected, the aye-aye uses its large, continuously growing incisors to gnaw through the tree’s exterior and extract the larvae within using the flexible middle finger ( Erickson 1991 ; Soligo 2005 ).…”