Acoustic Signals and Speciation: The Roles of Natural and Sexual Selection in the Evolution of Cryptic Species

“Furthermore, these correlations may ultimately provide a powerful explanatory framework for determining why mouse lemur species are ‘cryptic’, sensu Jones (1997).”

“Detailed studies on morphology, ecology, echolocation (reviewed by Jones 1997) and gene £ow are required in order to resolve the species status in such cases.”

“Among closely related species, mating signals are often more divergent than morphological, genetic, or other behavioral traits (Miller 1996; Jones 1997; Wells and Henry 1998; Irwin et al. 2001).”

“For example, partitioning of foraging habitat, in the absence of apparent differences in wing morphology (Jones 1997), was identified among the recently separated cryptic Pipistrellus species, whereby P. pygmaeus selects riparian habitats, while P. pipistrellus prefers a wide range of habitats…”

“…pipistrelles (45 kHz vs. 55 kHz) had been recorded previously within this species complex (Zingg 1990), but it is only through refined ecological and genetic research that the existence of a second species, P. pygmaeus (Leach 1825), could be proved (Barlow 1997; Barlow & Jones 1997; Barratt et al .”

“Closely related species often differ dramatically in the signals that they use to communicate, and these differences might play a central role in causing reproductive isolation (West-Eberhard, 1983; Henry, 1985; Jones, 1997; Slabbekoorn & Smith, 2002a; Mendelson & Shaw, 2005; Price, 2008).”

“Natural selection, such as adaptation to a different acoustical environment, sexual selection or random changes may cause population differences in song (West-Eberhard, 1983; Andersson, 1994; Butlin, 1995; Jones, 1997; Price, 1999).”

“The scenario of sympatric speciation, further discussed by Barrat et al. (1997) and Jones (1997) , predicts that a bimodality of echolocation calls would result from the character displacement within an ancestral population and that just this was the first step in the speciation story.”

“M signals mediate successful breeding and, therefore, are often affected by strong selective forces that may lead to adaptation and reproductive isolation (1, 2).”

“Central to the acoustic resource partitioning hypothesis is the relationship between call frequency and the size of prey that can be detected (Barclay 1986; Barclay & Brigham 1991; Jones 1997).”

“In contrast, species-specific recognition of advertisement calls plays an important role for reproduction in cryptic and dispersed living species where females and males have to find each other for courtship and mating [12].”

“…special skills or sophisticated techniques to uncover or assess (for recent examples from diverse groups, see Paterson 1991, Sweeney and Funk 1991, Vrijenhoek et al. 1994, Bernardi and Goswami 1997, Green et al. 1997, Jones 1997, Wilcox et al. 1997, Jackson and Resh 1998, Baric andSturmbauer 1999).”

“…that assortative mating is important early in speciation appears to result from two patterns in nature: First, traits involved in mate choice and other social dynamics are often the most noticeably divergent traits between populations (e.g., Jones 1997; Irwin et al. 2001; Masta and Maddison 2002).”

“In recent years, the identification of increasing numbers of cryptic species of bats has led to the assertion that the number of bat species currently described might be a substantial underestimate of bat diversity (Jones, 1997; Jones & Barlow, 2004).”

“…understanding of this narrow analysis sonar system, although the reason for using such high frequencies remains unclear (Fenton & Fullard, 1979; Fullard, 1987; Schnitzler, 1987; Vater, 1987; Heller & Helversen, 1989; Neuweiler, 1989, 1990a; RuÈ bsamen & SchaÈfer, 1990a,b; Jones, 1995, 1996, 1997).”

“nocturnal and active high in the air) makes them difficult to study in the wild [21].”

“Our study only tested sexual selection on echolocation calls as previously suggested [15–17,63,64] but given the rich repertoire of social calls in bats (e.”

“Nowadays, Italy is home to 34 bat species [30–33] but, as a general condition for this group of mammals, many taxa are nearly or completely indistinguishable morphologically, acoustically or biometrically [11,34–37].”

“Call frequency can dictate the size of detected prey (acoustic resource partitioning hypothesis; Barclay & Brigham, 1991; Jones, 1997) as well as the foraging habitat (Kingston et al.”

“…populations is not unusual, having been revealed in other recent studies where molecular work has uncovered many cryptic species, for example, in bats (Jones and van Parijs 1993; Jones 1997), fish (Colborn et al. 2001), corals (van Oppen et al. 2001), and copepods (Rocha-Olivares et al. 2001).”

“Cryptic diversity is predicted to be relatively common in bats, especially in Hipposideridae and Rhinolophidae, which have highly specialized echolocation systems that potentially constrain social communication (Jones, 1997).”

“Bats are often difficult to catch, and species identification of a captured bat may not be easy, especially for cryptic species (Jones 1997, Jones and Barratt 1999, Wicht et al. 2003).”

“Morphologically cryptic species complexes are common among all mammal groups, and bats are particularly prone to this kind of misclassification given their small size, elusive habits, morphological convergences, and subtle differences (Jones 1997; Mayer and von Helversen 2001; Clare et al.”

“In some species, a ‘lek’ system exists, with males advertising themselves by calling from the roost (Nyctalus noctula: Sluiter and Van Heerdt, 1964) or performing songflights (Pipistrellus pipistrellus and Pipistrellus pygmaeus: Lundberg and Gerell, 1986; Jones, 1997).”

“For instance, selective pressures for acoustic divergence and speciation could involve the influence of call frequency on echo strength from acoustic targets of different sizes and thus prey selection (Jones, 1997).”

“Cryptic species, defined as ecologically and/or genetically 56 distinct species with very similar morphology (Jones, 1997), pose a challenge to 57 understanding species distributions as they bring the need to redefine what was 58 once thought to be a single species’ distribution and environmental…”

“On the other hand, small interspecific differences in frequency of echolocation calls could be responsible for differing prey selection (Jones 1997).”

“While bats calling at higher frequencies are expected to catch smaller insects with more efficiency, those emitting at lower frequencies will target larger insects more successfully (Jones 1997; Kingston et al. 2001).”

“First, acoustic differentiation can be the consequence of genetic drift and or founder effects in isolated populations, or selection within communities (Jones, 1997).”

“…tool for determining species limits and has allowed the recognition of allopatric taxa with distinct vocalizations as species rather than subspecies, especially in elusive and morphologically similar groups (Jones, 1997; Isler, Isler & Whitney, 1999; Isler et al., 2001; Alstr€om & Ranft, 2003).”

“However, cryptic species of birds were once considered rare due to the perceived importance of vision in the recognition of sexual characteristics (Jones, 1997).”

“These cryptic species all co-occurred and such differences in sensory traits may be important isolating mechanisms between species [63] leading to resource partitioning and subsequent genetic divergence.”

“Among those that are often considered important are: (1) ecological selection, either directly as a result of habitat features that affect sound transmission (the ‘acoustic adaptation hypothesis’, Morton 1975; see also Wiley & Richards 1983; Endler 1992; Forrest 1994; Jones 1997; Patten et al. 2004; Seddon 2005; Nicho…”

“Advocates of one view (e.g., Jones, 1997 ) contend that adaptive, ecological divergence always precedes sexual selection in the origin of cryptic species.”

“Most cryptic bat species, identified through molecular techniques, cannot be identified using external morphology but often do show other distinguishing characters, either in echolocation call [12–14] or more subtle morphological characters such as cranial morphology or tragus shape [15,16].”

“Cryptic species are a group of species that are morphologically alike and hence difficult to distinguish based on external features, despite being genetically distinct (Jones, 1997).”

“In contrast, lower frequencies are associated with foraging in more open areas [70].”

“Many bat species have gone undocumented over time (Jones 1997; Kunz and Parsons 2009; Altringham 2011), especially cryptic species—defined as two or more closely related species that could be easily misidentified due to their morphological similarity (Bickford et al. 2007).”

“…allowing identification of competitors, predators and prey, whereas the recognition of conspecifics is a prerequisite for any species-specific interactions, especially for mate choice (Jones, 1997; Sandoval, M endez, & Mennill, 2013; Slabbekoorn & Smith, 2002; Wilkins, Seddon, & Safran, 2013).”

“Traditionally, bats have been identified based on morphological characters or biometric measurements [4, 5], and subsequently by echolocation acoustic analysis [6].”

“Pip i - strelle bats frequently emit agonistic social calls at foraging sites to repel conspecifics especially at low insect densities (Miller and Degn, 1981; Racey and Swift, 1985; Barlow and Jones, 1997b).”

“Many studies have been carried out to investigate coexistence in morphologically similar sympatric species of bats (Woodsworth, 1981; Herd & Fenton, 1983; Saunders & Barclay, 1992; Arlettaz, Perrin & Hausser, 1997; Jones, 1997; Arlettaz, 1999).”

“Given that they are strictly nocturnal, theory [13-15] would predict that mouse lemurs will emphasize olfactory and auditory communication signals over visual signals, as has been demonstrated for other nocturnal primates [1,2], [5,6], [16-18].”

“The distinction between species appears to be possible because acoustic signalling may be more flexible than morphology [17].”

“Pressures leading to social call divergence are also evident in the sympatric pipistrelles P. pipistrellus and P. pygmaeus (Barlow & Jones, 1997a; Russo & Jones, 2000).”

“…evolutionary lability, acoustic signals have been proposed to play an important role in the formation of pre-zygotic reproductive barriers and may facilitate or even drive the process of speciation (Blair, 1958; Jones, 1997; Slabbekoorn & Smith, 2002; Price, 2008; Wilkins, Seddon & Safran, 2013).”

“Hidden or cryptic species are defined as genetically- and/or ecologically-distinct species that are almost indiscernible in their morphology (Jones 1997).”

“On the other hand, stochastic (or “neutral”) forces, such as sexual or social selection [21, 22] or more commonly, genetic drift and mutation [13, 23–25] could be the driving initiators for signal divergence.”

“Such variation in echolocation frequency has the capacity to limit social interactions in echolocating bats (Jones 1997).”

“The discovery of crypic species on the basis of differences in acoustic signal structure is occurring in other taxa as well, including insects and mammals (Henry 1994, Jones 1997).”

“The prey detection hypothesis suggests that differences in echolocation frequencies may cause differentiation in prey sizes and that highfrequency calls are more sensitive to detecting smaller prey items (Barclay and Brigham, 1991; Jones, 1997).”

“In addition, no support has been presented for indirect selection in crickets due to pleiotropic effects that link song differentiation as a by-product to ecological or morphological adaptions to the environment (Otte 1992; Jones 1997; Podos 2001).”

“Differences in songflight calls and social calls between the phonic types were demonstrated by Barlow and Jones (1997), and their separation in time of mating suggested their reproductive isolation (Park et al., 1996).”

“In non–vocal learners, species divergence among isolated populations could emerge from selective forces such as ecology and mate choice, or could arise as a result of non-selective forces such as genetic drift (Jones 1997, Podos et al.”

“Cryptic species are fairly common in echolocating bats [21].”

“Consequently, several cryptic bat species (ecologically and/or genetically distinct species with similar morphology (Jones 1997)) have recently been identified worldwide (e.g. Chadès et al. 2008; Kaliontzopoulou et al. 2011; Boratynski et al. 2012).”

“In recent years, molecular, acoustic, behavioral, and morphological analyses have revealed a number of cryptic bat species within previously unsuspected taxa (Jones, 1997; Jones & Barlow, 2004; Kingston et al., 2001; Russo & Jones, 2000; Thabah et al., 2006).”

“…reproductive isolation, such as the infestation rate of endosymbiotic intracellular Wolbachia spp. bacteria (Zhang et al., 2022), sexual selection (Jones, 1997) or allopatry (Lukhtanov et al., 2015); (b) niche separation on an axis that does not include morphological factors (bioacoustics, host…”

“isolation through mechanisms that cannot be discerned or detected [6].”

“Disruptive ecological selection commonly acts on echolocation frequencies of bats in association with prey size specializations (Jones, 1997), and simple body size divergence in bats has extraordinary importance for trophic niche partitioning and stable coexistence of sympatric species (Andreas et…”

“Auditory signals used to delimit territory, such as made by bats, whales, lemurs and deer, are useful tools for species delimitation as well, especially to keep morphologically similar species apart (Jones 1997).”

“Geographic variation in mating calls is also documented in mammals (Jones 1997; Campbell et al.”