Fig 1 - available from: Nature Communications
This content is subject to copyright. Terms and conditions apply.
Two equally parsimonious hypotheses for the origination of laryngeal echolocation in bats. The unshaded side depicts the two origins hypothesis and predicts that laryngeal echolocation originated in the common ancestor to the Emballonuroidea, Noctilionoidea, and Vespertilionoidea and again in the Rhinolophoidea. The shaded side depicts the single origin hypothesis, which predicts laryngeal echolocation was present in the common ancestor of all bats and lost in the Pteropodidae. Middle column displays (top to bottom) five 30-35 g species from each of these major groups: Cynopterus brachyotis (non-echolocating, phytophagous), Rhinolophus hildebrandti (echolocating, predatory), Taphozous melanopogon (echolocating, predatory), Tonatia evotis (echolocating, predatory), Nyctalus noctula (echolocating, predatory). Please note that bats with constant frequency (CF), multi-harmonic frequency-modulated calls (MH) and fundamental harmonic frequency modulated calls (DH) (i.e., most energy in fundamental harmonic) are found in both suborders of bats. Photographs by Brock Fenton and Signe Brinkløv
Source publication
Substantial evidence now supports the hypothesis that the common ancestor of bats was nocturnal and capable of both powered flight and laryngeal echolocation. This scenario entails a parallel sensory and biomechanical transition from a nonvolant, vision-reliant mammal to one capable of sonar and flight. Here we consider anatomical constraints and o...
Contexts in source publication
Context 1
... we found no differences between foraging categories with respect to the absolute masses of the auditory brain regions: absolute inferior colliculus size (F = 0.323, p = 0.946) and absolute auditory nucleus size (F = 0.043, p = 0.992), which remain similar across these three categories (Supplementary Table 1). Neither did we observe any differences in the sizes of auditory brain regions in modern bats relative to the common ancestor (inferior colliculus: N = 84; AS = 12.93 mg, CI = 9.09, 18.4; auditory nucleus: N = 84; AS = 5.7 mg, CI = 4.08, 7.97) ( Fig. 3; Supplemen- tary Fig. 1; Supplementary Table ...
Context 2
... also confirmed that pteropodids have absolutely larger eyes than do laryngeal echolocators (F = 149.248, p = 0.001; Supple- mentary Table 1), and compared to the AS estimate at the root node, this suggests a trend of increasing eye size in pteropodids and possible reduction in eye size in most extant laryngeal echolocating bats ( Fig. 3; Supplementary Fig. 1). We also found that in relative terms, the non-laryngeal echolocating pteropodids had larger eyes than laryngeal echolocating bats, regardless of diet (F = 88.362, p < 0.001) (Supplementary Table 2) or call type (absolute: F = 136.18, p = 0.001; relative: F = 146.86, p = 0.001) (see Supplementary Tables 3 and ...
Context 3
... comparative analyses lend strong support to the already well- supported hypothesis that the common ancestor of bats was a small (~20 g), predatory, laryngeal echolocator 5,12,37 . Specifically, a bat that took flying insects on the wing at night 5 and roosted externally, rather than deep in caves. Our results, thus, also support the conclusion that LE has been lost, rather than never gained, in the family Pteropodidae 8 (Figs. 1-3). They also indicate that a switch to a phytophagous diet occurred at least twice in bats since their origin, once in the pteropodids (Yinpterochir- optera) and once or more within the laryngeal echolocating family Phyllostomidae (Yangochiroptera) 44 (Fig. ...
Context 4
... and eye mass were positively correlated with body mass. Thus, we generated phylogenetic residuals for log-transformed brain mass, eye mass, and brain region masses on body mass, and tested for differences in these residuals across our four call type categories and our three foraging categories. Summaries for the results are provided in-text and in Supplementary Tables 1-6. We also used Pagel's binary character correlation test to explored whether there were significant correlations between where bats roost (i.e., internally, externally) and (i) absolute and relative eye size or (ii) echolocation call types 74 . Further, using the same test, we tested the prediction that among predatory bats, there would be a significant correlation between CF echolocation and the loss of functionality in SWS opsin genes. Last, we plotted regressions of log transformed eye mass on body mass in the five most species rich bat families, while accounting for the phylogenetic non- independence among ...
Context 5
... better understand vertebrate brain evolution, it is now established that we should consider not only brain and brain region size in relative terms, but in terms of absolute size. This is because absolute size better reflects processing power, neural investment, and information use 48 . Strikingly, although we con- firmed that phytophagous species have relatively larger brains 40- 42 and non-auditory brain regions than today's predatory bats 41,43 , and than the ancestral bat (Supplementary Table 2; Supplementary Fig. 2), we found that the ancestral bat's auditory brain regions were of the same relative size as in extant predatory bats and had auditory regions roughly the same absolute size as those found in today's LE bats ( Fig. 3; Supplementary Table 1; Supplementary Fig. ...
Context 6
... better understand vertebrate brain evolution, it is now established that we should consider not only brain and brain region size in relative terms, but in terms of absolute size. This is because absolute size better reflects processing power, neural investment, and information use 48 . Strikingly, although we con- firmed that phytophagous species have relatively larger brains 40- 42 and non-auditory brain regions than today's predatory bats 41,43 , and than the ancestral bat (Supplementary Table 2; Supplementary Fig. 2), we found that the ancestral bat's auditory brain regions were of the same relative size as in extant predatory bats and had auditory regions roughly the same absolute size as those found in today's LE bats ( Fig. 3; Supplementary Table 1; Supplementary Fig. ...
Context 7
... also confirm relative brain size is greater in phytophagous bats (i.e., the pteropodids and the laryngeal echolocating phyto- phagous phyllostomids) than today's predatory bats [40][41][42]45 (Supplementary Table 2; Supplementary Fig. 2), and compared to Fig. 2 The ancestral state estimates of call types and foraging categories. a The echolocation signals of bat species (N = 183) were categorized as (i) constant frequency (CF), (ii) multi-harmonic calls (MH), (iii) frequency modulated calls dominated by the fundamental harmonic (DH), or non-laryngeal (NLE, i.e., pteropodids). Models of evolution were compared using AICc scores and the character states for ancestral call types were estimated under an equal rates model of evolution. These marginal ancestral states (i.e., the empirical Bayesian posterior probabilities) have been overlain on the phylogeny. We find support for a multi-harmonic ancestral call type (Bayesian posterior probabilities: CF: <0.001; MH: >0.999; DH: <0.001; MLE: <0.001). b Bats were also categorized as (i) predatory laryngeal echolocators (ALE), (ii) phytophagous laryngeal echolocators (PLE) and (iii) phytophagous non-laryngeal echolocators (PNLE). Models of evolution were compared using AICc scores and the character states for ancestral call types were estimated under an equal rates model of evolution. These marginal ancestral states have been overlain on the phylogeny. Our results suggest that the ancestral bat was a predatory laryngeal echolocator (Bayesian posterior probabilities: ALE: >0.999; PLE: <0.001; PNLE: <0.001) the common ancestor. This trend is largely due to enlargement of the olfactory bulb, hippocampus, and neocortex in phytophagous bats 41,43 ( Fig. 3; Supplementary Fig. 1). Further, our analyses demonstrate the ancestral bat had a relatively larger brain than some, but not all, extant predatory bat lineages, perhaps recon- ciling a current point of contention 37,46 (Supplementary Fig. 2). Our results also support the hypothesis that this bat used multi- harmonic (MH) echolocation calls, and thus that constant- frequency (CF) and dominant-harmonic (DH) call designs are derived states 5,12,14,29 (Fig. ...
Context 8
... results also demonstrate that echolocation may have ori- ginated first in the progenitors of bats, and only rarely in any vertebrate group thereafter 26,54 , not simply because they were pre-adapted for a sonar solution, but also because they were constrained by a small body 37,47 (Fig. 3), and thus skull and orbit size 35 , from instead realizing a vision-based solution. That is, while our AS reconstruction indicates that the ancestral bat had relatively and absolutely larger eyes (~3 mm diameter) than most extant LE bats ( Fig. 3; Supplementary Fig. 2; Supplementary Data 1), these same results reveal that their eyes were both relatively and absolutely smaller than those of all extant pter- opodid species, including those pteropodid species smaller in body size than the ancestral bat (i.e., all extant pteropodid species have eyes >5 mm diameter, while the smallest species weigh ~15 g; Fig. 3; Supplementary Figs. 1, 2). As we outline below, verte- brate eyes of the size estimated for the ancestral bat would be, then and now, too small to allow for the successful aerial pursuit of even undefended flying insects at ...
Context 9
... results suggest to us that pteropodids have apparently maintained auditory brain regions of the same absolute size as the Fig. 3 The ancestral states of bats versus modern foraging categories. The ancestral states (maximum likelihood estimate of the root node) of six continuous traits considered in this study are shown with 95% confidence intervals. The tree was re-rooted at each internal nodes and contrasts state at the root was computed each time. AS estimate at the root compared to extant foraging categories for: a body mass (N = 183), b eye mass (N = 183), c neocortex mass (N = 149), d superior colliculus mass (N = 84), e inferior colliculus mass (N = 84), and f auditory nucleus mass (N = 84). The ancestral state range of eye mass and non-auditory brain regions (b-d) suggest an increase in pteropodids, while those of the auditory regions (e, f) suggest a basic auditory brain design has been conserved in all bats. We found that the auditory regions (i.e., inferior colliculus, auditory nucleus) were the only brain regions that did not differ between the ancestral bat and today's species (see also Supplementary Fig. 1), supporting the notion that the ancestral bat had an auditory brain sufficient for echolocation common ancestor and extant LE bats ( Fig. 3; Supplementary Table 1; Supplementary Fig. 1). This lends support to the hypothesis that LE was lost, rather than never present, in this phytophagous lineage (Fig. 2a), as do several other lines of evi- dence. During prenatal cochlear development, pteropodids exhibit a rapid increase in cochlea size, similar to laryngeal echolocators and faster than other mammals 8 . They are also more sensitive to high frequency sounds than are similar-sized terres- trial mammals 9,26 . Indeed, the echolocation calls of most bats have peak frequencies between 20-60 kHz 12,15,50 , well within most pteropodids' auditory limits 9,51 . Further, genetic vestiges suggest ancient biosonar abilities in the pteropodids 10 . While LE is unknown in extant pteropodids-as is the case for echolocation of any kind in almost all ~200 pteropodid species-the biosonar-based orientation abilities of the tongue-clicking pter- opodid, Rousettus aegyptiacus, have recently been recognized as being more sophisticated than previously thought 25 . Furthermore, more rudimentary echo-based orientation has now been experi- mentally supported in at least two other pteropodid genera, based on wing clicks potentially used in nature for finding suitable roosting places in dark caves 52,53 . Taken together, all of the above suggests that not only was LE lost, rather than never present, in the Pteropodidae, but that the foundations for chiropteran echoloca- tion may not have regressed entirely and instead remain available to be built upon in this lineage. Indeed, this has, perhaps, happened several times already (see Fig. 3 in ref. 53 ...
Context 10
... results suggest to us that pteropodids have apparently maintained auditory brain regions of the same absolute size as the Fig. 3 The ancestral states of bats versus modern foraging categories. The ancestral states (maximum likelihood estimate of the root node) of six continuous traits considered in this study are shown with 95% confidence intervals. The tree was re-rooted at each internal nodes and contrasts state at the root was computed each time. AS estimate at the root compared to extant foraging categories for: a body mass (N = 183), b eye mass (N = 183), c neocortex mass (N = 149), d superior colliculus mass (N = 84), e inferior colliculus mass (N = 84), and f auditory nucleus mass (N = 84). The ancestral state range of eye mass and non-auditory brain regions (b-d) suggest an increase in pteropodids, while those of the auditory regions (e, f) suggest a basic auditory brain design has been conserved in all bats. We found that the auditory regions (i.e., inferior colliculus, auditory nucleus) were the only brain regions that did not differ between the ancestral bat and today's species (see also Supplementary Fig. 1), supporting the notion that the ancestral bat had an auditory brain sufficient for echolocation common ancestor and extant LE bats ( Fig. 3; Supplementary Table 1; Supplementary Fig. 1). This lends support to the hypothesis that LE was lost, rather than never present, in this phytophagous lineage (Fig. 2a), as do several other lines of evi- dence. During prenatal cochlear development, pteropodids exhibit a rapid increase in cochlea size, similar to laryngeal echolocators and faster than other mammals 8 . They are also more sensitive to high frequency sounds than are similar-sized terres- trial mammals 9,26 . Indeed, the echolocation calls of most bats have peak frequencies between 20-60 kHz 12,15,50 , well within most pteropodids' auditory limits 9,51 . Further, genetic vestiges suggest ancient biosonar abilities in the pteropodids 10 . While LE is unknown in extant pteropodids-as is the case for echolocation of any kind in almost all ~200 pteropodid species-the biosonar-based orientation abilities of the tongue-clicking pter- opodid, Rousettus aegyptiacus, have recently been recognized as being more sophisticated than previously thought 25 . Furthermore, more rudimentary echo-based orientation has now been experi- mentally supported in at least two other pteropodid genera, based on wing clicks potentially used in nature for finding suitable roosting places in dark caves 52,53 . Taken together, all of the above suggests that not only was LE lost, rather than never present, in the Pteropodidae, but that the foundations for chiropteran echoloca- tion may not have regressed entirely and instead remain available to be built upon in this lineage. Indeed, this has, perhaps, happened several times already (see Fig. 3 in ref. 53 ...
Context 11
... results suggest to us that pteropodids have apparently maintained auditory brain regions of the same absolute size as the Fig. 3 The ancestral states of bats versus modern foraging categories. The ancestral states (maximum likelihood estimate of the root node) of six continuous traits considered in this study are shown with 95% confidence intervals. The tree was re-rooted at each internal nodes and contrasts state at the root was computed each time. AS estimate at the root compared to extant foraging categories for: a body mass (N = 183), b eye mass (N = 183), c neocortex mass (N = 149), d superior colliculus mass (N = 84), e inferior colliculus mass (N = 84), and f auditory nucleus mass (N = 84). The ancestral state range of eye mass and non-auditory brain regions (b-d) suggest an increase in pteropodids, while those of the auditory regions (e, f) suggest a basic auditory brain design has been conserved in all bats. We found that the auditory regions (i.e., inferior colliculus, auditory nucleus) were the only brain regions that did not differ between the ancestral bat and today's species (see also Supplementary Fig. 1), supporting the notion that the ancestral bat had an auditory brain sufficient for echolocation common ancestor and extant LE bats ( Fig. 3; Supplementary Table 1; Supplementary Fig. 1). This lends support to the hypothesis that LE was lost, rather than never present, in this phytophagous lineage (Fig. 2a), as do several other lines of evi- dence. During prenatal cochlear development, pteropodids exhibit a rapid increase in cochlea size, similar to laryngeal echolocators and faster than other mammals 8 . They are also more sensitive to high frequency sounds than are similar-sized terres- trial mammals 9,26 . Indeed, the echolocation calls of most bats have peak frequencies between 20-60 kHz 12,15,50 , well within most pteropodids' auditory limits 9,51 . Further, genetic vestiges suggest ancient biosonar abilities in the pteropodids 10 . While LE is unknown in extant pteropodids-as is the case for echolocation of any kind in almost all ~200 pteropodid species-the biosonar-based orientation abilities of the tongue-clicking pter- opodid, Rousettus aegyptiacus, have recently been recognized as being more sophisticated than previously thought 25 . Furthermore, more rudimentary echo-based orientation has now been experi- mentally supported in at least two other pteropodid genera, based on wing clicks potentially used in nature for finding suitable roosting places in dark caves 52,53 . Taken together, all of the above suggests that not only was LE lost, rather than never present, in the Pteropodidae, but that the foundations for chiropteran echoloca- tion may not have regressed entirely and instead remain available to be built upon in this lineage. Indeed, this has, perhaps, happened several times already (see Fig. 3 in ref. 53 ...
Context 12
... predatory bats, all of which laryngeally echolocate, we found that those that produce strictly MH calls had relatively larger eyes than did DH and CF bats (Fig. 4 Table 6). Our results and the conclusions of researchers before us 5,12,14,21 indicate that MH calls most closely resemble those of the ancestral bat (Fig. 2b) and are closest in structure to those of non-echolocating terrestrial mammals 12,14 . Our results therefore suggest that although absolute and relative eye size has decreased in all extant lineages of predatory bats as compared to the common ancestor (Fig. 3, Supplementary Fig. 1, Supplementary Fig. 2), relative eye size has decreased least in MH bats and most in DH and CF bats. Our analyses suggest that this difference is not accounted for by roost preference, and suggest that the exclusively predatory emballonurids have eyes at least as large as those of phyllostomids (Fig. ...
Context 13
... larger eyes but also have relatively larger skulls than otherwise similarly sized diurnal aerial insectivorous birds 55,57 , and have average body weights of ~50 g or more 47 . Thus, we suggest the ancestral bats' skull may have been too small to afford eyes large enough to allow sufficient sensitivity and resolution to guide and control flight at low light intensities and successfully track and capture flying insects. Under this scenario, the reduction in relative eye size in extant LE bats as compared to ancestral bat would reflect a greater reliance on more sophisti- cated echolocation over evolutionary time and a reduced reliance on vision (Fig. 3, Supplementary Fig. 1). The loss of a functional SWS opsin gene in CF bats (Supplementary Table 7; Supple- mentary Fig. 3), likely resulting in monochromatic rather than dichromatic vision in these sophisticated echolocators 36 , supports the plausibility of this viewpoint. Conversely, the sensory divergence of the pteropodids away from early LE and towards a primarily vision-based solution reflects a transition from an insect to plant-based diet. This shift to relatively larger, energy-rich, stationary food times would have allowed for larger bodies, skulls, and eyes, and selected for larger brain regions associated with vision, olfaction, and spatial memory 45 . LE likely regressed due to physiological cost and lack of stabilizing selection, given the reduced benefit of sonar for locating stationary ripe fruit and flowers relative to detecting and tracking small moving insects. Notably, almost no phytophagous bat is known to use derived (i.e., CF or DH) echolocation calls. The pteropodid Rousettus aegyptiacus is a tongue-clicking echo- locator, while all phytophagous phyllostomids, but one 58 , use MH call designs (Supplementary Data ...
Context 14
... larger eyes but also have relatively larger skulls than otherwise similarly sized diurnal aerial insectivorous birds 55,57 , and have average body weights of ~50 g or more 47 . Thus, we suggest the ancestral bats' skull may have been too small to afford eyes large enough to allow sufficient sensitivity and resolution to guide and control flight at low light intensities and successfully track and capture flying insects. Under this scenario, the reduction in relative eye size in extant LE bats as compared to ancestral bat would reflect a greater reliance on more sophisti- cated echolocation over evolutionary time and a reduced reliance on vision (Fig. 3, Supplementary Fig. 1). The loss of a functional SWS opsin gene in CF bats (Supplementary Table 7; Supple- mentary Fig. 3), likely resulting in monochromatic rather than dichromatic vision in these sophisticated echolocators 36 , supports the plausibility of this viewpoint. Conversely, the sensory divergence of the pteropodids away from early LE and towards a primarily vision-based solution reflects a transition from an insect to plant-based diet. This shift to relatively larger, energy-rich, stationary food times would have allowed for larger bodies, skulls, and eyes, and selected for larger brain regions associated with vision, olfaction, and spatial memory 45 . LE likely regressed due to physiological cost and lack of stabilizing selection, given the reduced benefit of sonar for locating stationary ripe fruit and flowers relative to detecting and tracking small moving insects. Notably, almost no phytophagous bat is known to use derived (i.e., CF or DH) echolocation calls. The pteropodid Rousettus aegyptiacus is a tongue-clicking echo- locator, while all phytophagous phyllostomids, but one 58 , use MH call designs (Supplementary Data ...
Context 15
... and categorical AS reconstruction. We used phytools (v. 0.5-38) to reconstruct ASs 74 for all log-transformed continuous variables, which we then anti- logged. The confidence intervals of the ancestral estimates for each variable were then compared to species-level modern categories (Fig. 1). We also used AICc scores to determine the most appropriate model of rate evolution and with phytools (v. 0.5-38), estimated the scaled likelihoods of each AS 74 at the root node for our three foraging categories, four call type categories, two roost categories and for the functionality of the SWS opsin gene. The probabilities of these ancestral character estimates have been overlain on the phylogenies in Fig. 2 and Supplementary Fig. ...
Context 16
... reconstructed ASs of body and brain mass. These reconstructions suggest that the ancestral bat was ~20 g, roughly the mean size of today's laryngeal echolocating bats, and smaller than most extant pteropodid bats ( Fig. 3; Supplementary Fig. 1), with a relative brain mass >20% smaller than that of extant pteropodid species (body mass: N = 183, root AS = 18.55 g, 95% confidence interval (CI) = 7.18 (lower limit), 47.91 (upper limit); brain mass: N = 183; AS = 428.33 mg, CI = 229.59, 799.08), confirming a previous report 37 . For comparison with AS reconstructions of auditory brain regions (see below) and for comparison with modern day bats, we also reconstructed the ASs of several non-auditory brain region masses associated with sensory information processing (neocortex: N = 149; AS = 94.15 mg, CI = 61.25, 144.71; hippocampus: N = 149; AS = 26.53 mg, CI = 18.24, 38.58; olfactory bulb: N = 149; AS = 9.02 mg, CI = 5.8, 14.05; superior colliculus: N = 84; AS = 6.66 mg, CI = 4.69, 9.45; Fig. 3; Supplementary Fig. ...
Context 17
... reconstructed ASs of body and brain mass. These reconstructions suggest that the ancestral bat was ~20 g, roughly the mean size of today's laryngeal echolocating bats, and smaller than most extant pteropodid bats ( Fig. 3; Supplementary Fig. 1), with a relative brain mass >20% smaller than that of extant pteropodid species (body mass: N = 183, root AS = 18.55 g, 95% confidence interval (CI) = 7.18 (lower limit), 47.91 (upper limit); brain mass: N = 183; AS = 428.33 mg, CI = 229.59, 799.08), confirming a previous report 37 . For comparison with AS reconstructions of auditory brain regions (see below) and for comparison with modern day bats, we also reconstructed the ASs of several non-auditory brain region masses associated with sensory information processing (neocortex: N = 149; AS = 94.15 mg, CI = 61.25, 144.71; hippocampus: N = 149; AS = 26.53 mg, CI = 18.24, 38.58; olfactory bulb: N = 149; AS = 9.02 mg, CI = 5.8, 14.05; superior colliculus: N = 84; AS = 6.66 mg, CI = 4.69, 9.45; Fig. 3; Supplementary Fig. ...
Context 18
... brain regions versus modern foraging categories. Phylogenetic analyses of variance (ANOVAs) indicate that pter- opodid bats are significantly larger than animal-eating bats (F = 40.353, p = 0.03; Supplementary Table 1). We also found that absolute brain, neocortex, hippocampus, and olfactory bulb sizes are significantly larger in pteropodids than in animal-eating bats (brain: F = 70.763, p = 0.009; neocortex: F = 55.618, p = 0.006; hippocampus: F = 82.641, p = 0.001; olfactory bulb: F = 85.068, p = 0.001; Supplementary Table 1). AS reconstructions suggest that these structures have become larger in pteropodids, while the neocortex and olfactory bulb may have become smaller in animal-eating species ( Fig. 3; Supplementary Fig. 1). We found that absolute superior colliculi are larger in pteropodid bats than in animal-eating bats (F = 26.937, p = 0.014; Supplementary Table 1) and larger in pteropodids compared to ancestral reconstructions, suggesting greater investment in visual tracking ( Fig. 3; Supplementary Fig. 1). For each of these traits, the phy- tophagous phyllostomids fell somewhere between the pteropodids and animal-eating bats, and did not differ from either of these groups significantly (Supplementary Table ...
Context 19
... brain regions versus modern foraging categories. Phylogenetic analyses of variance (ANOVAs) indicate that pter- opodid bats are significantly larger than animal-eating bats (F = 40.353, p = 0.03; Supplementary Table 1). We also found that absolute brain, neocortex, hippocampus, and olfactory bulb sizes are significantly larger in pteropodids than in animal-eating bats (brain: F = 70.763, p = 0.009; neocortex: F = 55.618, p = 0.006; hippocampus: F = 82.641, p = 0.001; olfactory bulb: F = 85.068, p = 0.001; Supplementary Table 1). AS reconstructions suggest that these structures have become larger in pteropodids, while the neocortex and olfactory bulb may have become smaller in animal-eating species ( Fig. 3; Supplementary Fig. 1). We found that absolute superior colliculi are larger in pteropodid bats than in animal-eating bats (F = 26.937, p = 0.014; Supplementary Table 1) and larger in pteropodids compared to ancestral reconstructions, suggesting greater investment in visual tracking ( Fig. 3; Supplementary Fig. 1). For each of these traits, the phy- tophagous phyllostomids fell somewhere between the pteropodids and animal-eating bats, and did not differ from either of these groups significantly (Supplementary Table ...
Similar publications
How echolocation and flight evolved in modern day bats is a compelling and largely unanswered question in biology. As laryngeal echolocation in bats is typified by a bony connection between the larynx and the auditory bulla via the hyoid apparatus, we developed an evolutionary‐developmental model of the hyoid to test hypotheses regarding the evolut...
Citations
... Fossil evidence (Speackman 2001;Brown et al. 2019) and recent phylogenetic reconstructions of genes encoding digestive enzymes associated with diet specialization (e.g., Emerling et al. 2018;Jiao et al. 2019) support the theory that early bats fed primarily on arthropods. Species in the suborder Yangochiroptera (including 14 families) underwent a niche displacement to nocturnal habits and developed an echolocation mechanism to navigate and locate their prey in the dark (Speackman 2001;Jones and Rydell 2003;Thiagavel et al. 2018)-in contrast, within the suborder Yingochiroptera, only the 6 families of the superfamily Rhinolophoidea converged on nocturnal habits and the development of echolocation. ...
Arthropod–bat interactions are often considered as a base model for studying factors underlying predator–prey coevolutionary processes. Bats developed ultrasonic echolocation to hunt, and in response some arthropods developed defense mechanisms such as ultrasonic hearing, allowing them to elude bat predators. The present study analyzes the feeding patterns of bats, focusing on sonic-auditory sensory mechanisms in predator–prey interactions. Next-generation DNA sequence data from fecal samples were used to analyze the diet of 17 bat species from Mexico. Arthropod prey taxa were classified according to their auditory traits, and echolocation data were recompiled from literature review. We: (i) classified arthropod families according to their hearing ability; (ii) estimated arthropod taxon richness and proportion in the diet of each bat species; and (iii) used multidimensional scaling, principal component analysis, and regression to analyze prey consumption patterns in relation to their auditory traits and in relation to echolocation characteristics of bats. Finally, we analyzed the relationship between foraging time and auditory characteristics of prey. Families with hearing organs correspond to the orders Lepidoptera and Orthoptera. We registered 20 families of Lepidoptera and 5 of Orthoptera—7 and 3 with hearing organs, respectively. Of these orders, families lacking ears were recorded in the diet of a few bat species. Our results support the allotonic frequency hypothesis predicting a difference in emission frequency intervals between predator and prey. However, we found that the consumption of earless moths is less frequent and is related to diurnal and twilight activity—hence, their consumption is limited to bat species foraging early. Results indicate bats feed on arthropod prey successfully despite the ultrasonic hearing ability of the prey. These results may be due to counteradaptations that allow maintenance of an asymmetric “arms race” between bats and eared insects that favors the predator.
... some rodents, hagfish and cavefish), where vision has degenerated as an adaptation to perpetual darkness [20,21]. This notion is supported by the evolutionary loss of echolocation in larger fruit-eating bats (Pteropodidae), which secondarily evolved large eyes with functional colour vision to exploit new diurnal foraging niches [22]. The apparent trade-off between investing in either echolocation or vision has likely resulted in large and non-insectivorous extant bats typically being more dependent on vision, whereas small insectivorous bats mostly rely on echolocation [22,23]. ...
... This notion is supported by the evolutionary loss of echolocation in larger fruit-eating bats (Pteropodidae), which secondarily evolved large eyes with functional colour vision to exploit new diurnal foraging niches [22]. The apparent trade-off between investing in either echolocation or vision has likely resulted in large and non-insectivorous extant bats typically being more dependent on vision, whereas small insectivorous bats mostly rely on echolocation [22,23]. Despite this, small extant insectivorous bats have maintained complex eye anatomy and display strong selection for the expression of photo-active opsin genes, suggesting functional vision [24,25]. ...
Most bats hunt insects on the wing at night using echolocation as their primary sensory modality, but nevertheless maintain complex eye anatomy and functional vision. This raises the question of how and when insectivorous bats use vision during their largely nocturnal lifestyle. Here, we test the hypothesis that the small insectivorous bat, Myotis daubentonii, relies less on echolocation, or dispenses with it entirely, as visual cues become available during challenging acoustic noise conditions. We trained five wild-caught bats to land on a spherical target in both silence and when exposed to broad-band noise to decrease echo detectability, while light conditions were manipulated in both spectrum and intensity. We show that during noise exposure, the bats were almost three times more likely to use multiple attempts to solve the task compared to in silent controls. Furthermore, the bats exhibited a Lombard response of 0.18 dB/dBnoise and decreased call intervals earlier in their flight during masking noise exposures compared to in silent controls. Importantly, however, these adjustments in movement and echolocation behaviour did not differ between light and dark control treatments showing that small insectivorous bats maintain the same echolocation behaviour when provided with visual cues under challenging conditions for echolocation. We therefore conclude that bat echolocation is a hard-wired sensory system with stereotyped compensation strategies to both target range and masking noise (i.e. Lombard response) irrespective of light conditions. In contrast, the adjustments of call intervals and movement strategies during noise exposure varied substantially between individuals indicating a degree of flexibility that likely requires higher order processing and perhaps vocal learning.
... To avoid signal overlap, some bats have evolved adaptations like Doppler shift compensation [4]. Due to flight and echolocation performance, peak frequency, bandwidth, and call duration have been linked to body size [35,48]. In this sense, bats that use high frequencies, broad bandwidths, and short calls are expected to forage in close areas, where they must be small for a better flight maneuverability [36,49]. ...
... These mechanisms would rely on flight and echolocation performance constrains and are exclusive of bats. In this sense, it has been even suggested that echolocation imposed a selective pressure on bats size, and that is why they would be small [35,48]. Because of the quick air attenuation of high-frequency sounds, and the weak signal given by small insects, the high-peak frequencies of echolocation calls can only detect these insects in a short range. ...
... It is also needed to look at the mode of evolution of call intensity and its correlation with the other acoustic parameters and body size. Frugivorous and nectarivore bats may have been able to overcome the echolocation constrain of size by utilizing other senses like vision and olfaction in foraging [48]. Pteropodidae (family with the biggest species of the Chiroptera order) could have even lost laryngeal echolocation, potentially allowing them to increase in size [48]. ...
Background
Body size and echolocation call frequencies are related in bats. However, it is unclear if this allometry applies to the entire clade. Differences have been suggested between nasal and oral emitting bats, as well as between some taxonomic families. Additionally, the scaling of other echolocation parameters, such as bandwidth and call duration, needs further testing. Moreover, it would be also interesting to test whether changes in body size have been coupled with changes in these echolocation parameters throughout bat evolution. Here, we test the scaling of peak frequency, bandwidth, and call duration with body mass using phylogenetically informed analyses for 314 bat species. We specifically tested whether all these scaling patterns differ between nasal and oral emitting bats. Then, we applied recently developed Bayesian statistical techniques based on large-scale simulations to test for the existence of correlated evolution between body mass and echolocation.
Results
Our results showed that echolocation peak frequencies, bandwidth, and duration follow significant allometric patterns in both nasal and oral emitting bats. Changes in these traits seem to have been coupled across the laryngeal echolocation bats diversification. Scaling and correlated evolution analyses revealed that body mass is more related to peak frequency and call duration than to bandwidth. We exposed two non-exclusive kinds of mechanisms to explain the link between size and each of the echolocation parameters.
Conclusions
The incorporation of Bayesian statistics based on large-scale simulations could be helpful for answering macroevolutionary patterns related to the coevolution of traits in bats and other taxonomic groups.
... There remain multiple scenarios for the evolution of echolocation, either "that advanced echolocation evolved once in the common ancestor of extant bats…but was lost in pteropodids, or that advanced echolocation evolved independently several times in bats, at least once in non-crown bats and twice in extant bat lineages. " [4(p33)] Ultimately, laryngeal echolocation may best be considered as a suite of traits, some of which may have preceded others over evolutionary time [7]. ...
... For example, Vielasia had small eyes that would be unlikely to permit visual hunting at night (further supporting its reliance on echolocation). (see [6], [7]) Long bone analyses suggest the species had an adult body mass of ~ 19 g and mandible morphology indicating the species was likely insectivorous, an estimate remarkably similar to previous predictions of the common ancestor of extant bats [8]. Aside from morphometrics, exceptional opportunity lies in the fact that the remains of at least 23 individuals were discovered together in cave sediment including at least one juvenile. ...
Sister to the Chiroptera crown-clade, the 50 million year old Vielasia sigei is suggested to have used laryngeal echolocation based on morphometric analyses. We discuss how Vielasia’s discovery influences our understanding of the evolution of echolocation in bats and the insights fossils provide to the lives of extinct species.
... Fossil bat skull morphology suggests that the common ancestor of Chiroptera used echolocation, supporting the first scenario [12,13] (but see for an opposed view [14]). Furthermore, it has been reported that the relative size of auditory brain regions (e.g. the auditory cortex and inferior colliculus) of the chiropteran ancestor is equivariant to that of extant echolocating bats, supporting the first scenario as well [15]. A study that investigated the growth rate of the cochlea during bat embryogenesis showed that the cochlea in all lineages, including non-echolocating pteropodid bats, was significantly larger than that of non-echolocating mammals at its initial developmental stage, providing further support for the first scenario [16]. ...
... The 'single origin' scenario for the evolution of bat laryngeal echolocation has been dominant thus far, supported by the fact that fossil bats seem to possess the auditory apparatus necessary for echolocation [12,13,15,16] (figure 1). However, recent studies have shown that the echolocating rhinolophoid and yangochiropteran lineages have distinct anatomical structures and spatio-temporal morphogenetic patterns in their auditory apparatuses, while pteropodid auditory apparatuses are similar to those of non-bat mammals, supporting the 'dual origin' scenario [17,18] (figure 1). ...
The order Chiroptera (bats) is the second largest group of mammals. One of the essential adaptations that have allowed bats to dominate the night skies is laryngeal echolocation, where bats emit ultrasonic pulses and listen to the returned echo to produce high-resolution ‘images’ of their surroundings. There are two possible scenarios for the evolutionary origin of laryngeal echolocation in bats: (1) a single origin in a common ancestor followed by the secondary loss in Pteropodidae, or (2) two convergent origins in Rhinolophoidea and Yangochiroptera. Although data from palaeontological, anatomical, developmental and genomic studies of auditory apparatuses exist, they remain inconclusive concerning the evolutionary origin of bat laryngeal echolocation. Here we compared musculoskeletal morphogenesis of the larynx in several chiropteran lineages and found distinct laryngeal modifications in two echolocating lineages, rhinolophoids and yangochiropterans. Our findings support the second scenario that rhinolophoids and yangochiropterans convergently evolved advanced laryngeal echolocation through anatomical modifications of the larynx for ultrasonic sound generation and refinement of the auditory apparatuses for more detailed sound perception.
... Recent morphological studies have revealed that echolocation is central in shaping the diversification of bats, and in particularly noctilionoids (Arbour et al., 2019(Arbour et al., , 2021Hedrick et al., 2020;Sulser et al., 2022;Thiagavel et al., 2018). As part of their ecological adaptations for diverse foraging modes, these bats have evolved nearly the full range of bat echolocation call types, such as constant frequency, short broadband multiharmonic, narrowband multiharmonic, and short broadband fundamental harmonic (Davies, Bates, et al., 2013;Jones et al., 2013;Jones & Teeling, 2006;Sulser et al., 2022;Thiagavel et al., 2018). ...
... Recent morphological studies have revealed that echolocation is central in shaping the diversification of bats, and in particularly noctilionoids (Arbour et al., 2019(Arbour et al., , 2021Hedrick et al., 2020;Sulser et al., 2022;Thiagavel et al., 2018). As part of their ecological adaptations for diverse foraging modes, these bats have evolved nearly the full range of bat echolocation call types, such as constant frequency, short broadband multiharmonic, narrowband multiharmonic, and short broadband fundamental harmonic (Davies, Bates, et al., 2013;Jones et al., 2013;Jones & Teeling, 2006;Sulser et al., 2022;Thiagavel et al., 2018). They also vary in their reliance on echolocation, vision, and olfaction (Gracheva et al., 2011;Sadier et al., 2018;Schnitzler et al., 1994;Thies et al., 1998). ...
Sensory organs must develop alongside the skull within which they are largely encased, and this relationship can manifest as the skull constraining the organs, organs constraining the skull, or organs constraining one another in relative size. How this interplay between sensory organs and the developing skull plays out during the evolution of sensory diversity; however, remains unknown. Here, we examine the developmental sequence of the cochlea, the organ responsible for hearing and echolocation, in species with distinct diet and echolocation types within the ecologically diverse bat super‐family Noctilionoidea. We found the size and shape of the cochlea largely correlates with skull size, with exceptions of Pteronotus parnellii , whose high duty cycle echolocation (nearly constant emission of sound pulses during their echolocation process allowing for detailed information gathering, also called constant frequency echolocation) corresponds to a larger cochlear and basal turn, and Monophyllus redmani , a small‐bodied nectarivorous bat, for which interactions with other sensory organs restrict cochlea size. Our findings support the existence of developmental constraints, suggesting that both developmental and anatomical factors may act synergistically during the development of sensory systems in noctilionoid bats.
... A strong reliance on hearing and echolocation may be reflective of an adaptation for nocturnality, which typifies the vast majority of extant bats. In modeling for the common ancestor of bats, Thiagavel et al. (2018) assert that the eyes of ancestral bats were small, too small to aid in visual pursuit of aerial insects, and that these bats were small, volant, and already capable of laryngeal echolocation. Further, these authors observe that among extant bats, those with the most sophisticated echolocation abilities have the smallest eyes, suggesting that extant bats bear the stamp of a trade-off of vision and specialization for echolocation. ...
... One likely trend is a reduction in number and size of ethmoturbinals in this group. Combined with the observations of variable olfactory anatomy in other bat families, this finding is consistent with a hypothesis that ancestral bats had well-developed olfactory anatomy, and all extant families are undergoing adaptive changes to the midface that broadly reflect constraint on visual system and selection for anatomy facilitating echolocation (Thiagavel et al., 2018). ...
... The continued internal exploration of bat sensory systems will eventually allow a comprehensive picture of sensory ecomorphology in bats. As of now, the majority of our understanding is centered on auditory specialization and vision, and phylogenetic analyses suggest that echolocation is an ancestral feature of bats, and with a trade-off for reduced vision (Thiagavel et al., 2018); within bat families, there are "über" specialists in echolocation who appear to have the most extremely diminutive visual systems (Arbour et al., 2021;Thiagavel et al., 2018). This raises the question, are other sensory systems facilitated or constrained in bats? ...
This special issue of The Anatomical Record is inspired by and dedicated to Professor Kunwar P. Bhatnagar, whose lifelong interests in biology, and long career studying bats, inspired many and advanced our knowledge of the world's only flying mammals. The 15 articles included here represent a broad range of investigators, treading topics familiar to Prof. Bhatnagar, who was interested in seemingly every aspect of bat biology. Key topics include broad themes of bat development, sensory systems, and specializations related to flight and diet. These articles paint a complex picture of the fascinating adaptations of bats, such as rapid fore limb development, ear morphologies relating to echolocation, and other enhanced senses that allow bats to exploit niches in virtually every part of the world. In this introduction, we integrate and contextualize these articles within the broader story of bat ecomorphology, providing an overview of each of the key themes noted above. This special issue will serve as a springboard for future studies both in bat biology and in the broader world of mammalian comparative anatomy and ecomorphology.
... Neotropical noctilionoid bats include 248 species, 218 of which comprise the family Phyllostomidae (Fleming et al. 2020), commonly known as the Neotropical leaf-nosed bats. Most noctilionoid families are primarily insectivorous and divergence among lineages presents as subtle variation in body size, foraging style, and echolocation calls (Freeman 2000;Rolfe 2011;Baker et al. 2012;Thiagavel et al. 2018;Rodriguez-Durán and Rosa 2020). Although phyllostomids maintain the ancestral multi-harmonic echolocation calls, they have escaped strict insectivory and diversified into dietary niches that include nectar, fruit, vertebrates, and blood ( Fig. 1, also see Fig. 1 in Dumont et al. 2012). ...
... Analyses of character state evolution provide the clearest picture of correlated structural change both outside and within Phyllostomidae (Fig. 5 Our results align with the view that preadaptation in sensory systems played a leading role in the evolution of bats (Thiagavel et al. 2018;Davies et al. 2020) and the earliest phyllostomids experimented with foods beyond insects (Freeman 2000;Baker et al. 2012;Hedrick et al. 2020), while also demonstrating how sensory and mechanical abilities coevolve. ...
... Within phyllostomids, module coevolution supports This is the author's accepted manuscript without copyediting, formatting, or final corrections. It will be published in its final form in an upcoming issue of The American Naturalist, published by more specialized behaviors such as the ability to detect flowers and ripe fruits and to process nectar and hard fruits (Davies et al. 2013b(Davies et al. , 2013aThiagavel et al. 2018). Nectar feeding lineages exhibit elevated rates of evolution in the palate, face, and, to a lesser extent, the skull base and eye modules (Fig. 4, Sup. ...
Are bats really just what they eat? Oh well yes of course, plus a few parts per meal/mil. In this paper we sought to answer how interrelationships among different structures of the head may influence the evolution of a species, and how this can be associated with diet. After sampling a few sensory and mechanical structures from the Noctilionoid superfamily, we found that sensory systems evolved earlier and faster that most mechanical systems. This may have triggered a release from an insect based ancestral diet into plant based niches which were diverse. Phyllostomids explosively radiated into diverse diets following changes in the relationships among sensory and mechanical systems.
... These results support the prediction that species preying on vertebrates and invertebrates require large ranges of motion in order to capture and process large or agile prey. Our estimations of ancestral state suggest that insectivory is the ancestral condition in bats, as found in other studies (Thiagavel et al., 2018), and that intermediate ranges of head-neck motion are plesiomorphic. The lower ranges of motion, especially extension, seen in the frugivores appear to be more derived than the intermediate and high ranges in insectivores and carnivores (Fig. 6). ...
The primary functions of the tetrapod neck are to maintain head stability and facilitate head mobility. Both stability and mobility should be especially important during foraging. Head stability facilitates the function of the vestibulocochlear, auditory, and visual organs while mobility allows for the motion of that visual field as well as the mouth for food capture and processing. Species that rely on different resources should be under different selective pressures with regard to range of motion of the head and neck and the musculoskeletal morphologies that sustain them. Bats are useful model species to investigate these pressures because they display a wide variety of foraging behaviors. This study tests the hypothesis that dietary regime influences maximum ranges of motion found in the head and neck. To test this hypothesis, a dietarily diverse group of bats were caught in the field and their active ranges of head–neck motion were measured via photographs. Diet information was taken from the literature. Additionally, gross neck dimensions (mediolateral neck width and craniocaudal neck length) were measured using calipers. Phylogenetic statistical methods support the hypothesis and demonstrate that frugivorous species have much smaller ranges of head and neck motion. The results indicate that frugivorous species may require stiffness in their cervical spine in order to carry heavy fruits and maintain head stability simultaneously. Future work should investigate the anatomical differences in the head and neck among bats that influence this stiffness as well as other dietary behaviors that could be shaping the form and function of the head and neck. Bats possess a diverse array of dietary behaviors that have shaped their anatomy. This study demonstrates that species primarily relying on large, heavy fruits have stiff necks, possibly to maintain head stability while transporting food.
... For example, bats (Chiroptera), being the only extant mammals to have evolved powered flight, exhibit substantial constraints in body size (Jones, 1994;Moyers Arévalo et al., 2020). Other trade-offs in bats include those between the energetic demands associated with both echolocation and vision (Thiagavel et al., 2018). Similarly, beetle weaponry (i.e., horns and extreme mandibles) has evolved several times across the Coleoptera, and are generally used for male sparring (Emlen, 2000). ...
... Over the past 40 years, the field of evolutionary biology has further recognized the value of identifying constraints associated with development and how these mechanisms ultimately shape evolution (Cheverud, 1984;Conith et al., 2021;Gould, 1980;Holekamp et al., 2013;Pigliucci & Preston, 2004). The exploration of extreme traits has shed light on the constraints that may be present in a system and has been done so in various systems (Emlen, 2000;Gilbert et al., 2021;Goyens et al., 2015;Moyers Arévalo et al., 2020;Nijhout & Emlen, 1998;Thiagavel et al., 2018). Here, we build on this by examining how the development, and evolution, of an extreme trait can influence a unique, enigmatic lineagethe Bramidae. ...
The developmental process establishes the foundation upon which natural selection may act. In that same sense, it is inundated with numerous constraints that work to limit the directions in which a phenotype may respond to selective pressures. Extreme phenotypes have been used in the past to identify tradeoffs and constraints and may aid in recognizing how alterations to the Baupläne can influence the trajectories of lineages. The Bramidae, a family of Scombriformes consisting of 20 extant species, are unique in that five species greatly deviate from the stout, ovaloid bodies that typify the bramids. The Ptericlinae, or fanfishes, are instead characterized by relatively elongated body plans and extreme modifications to their medial fins. Here, we explore the development of Bramidae morphologies and examine them through a phylogenetic lens to investigate the concepts of developmental and evolutionary constraints. Contrary to our predictions that the fanfishes had been constrained by inherited properties of an ancestral state, we find that the fanfishes exhibit both increased rates of trait evolution and differ substantially from the other bramids in their developmental trajectories. Conversely, the remaining bramid genera differ little, both among one another and in comparison, to the sister family Caristiidae. In all, our data suggest that the fanfishes have broken constraints, thereby allowing them to mitigate trade‐offs on distinctive aspects of morphology. Morphospace of the combined juvenile and adult data sets, illustrating phenotypic change in morphospace throughout ontogeny from juvenile to adult. Fanfishes stand out among the Bramidae due to an extreme morphological adaptation and may provide opportunities to study how constraints are broken to allow expansion into new realms of phenotypic space.
