Social evolution in toothed whales

Two contrasting results emerge from comparisons of the social systems of several odontocetes with terrestrial mammals. Researchers have identified remarkable convergence in prominent features of the social systems of odontocetes such as the sperm whale and bottlenose dolphin with a few well-known terrestrial mammals such as the elephant and chimpanzee. In contrast, studies on killer whales and Baird's beaked whale reveal novel social solutions to aquatic living. The combination of convergent and novel features in odontocete social systems promise a more general understanding of the ecological determinants of social systems in both terrestrial and aquatic habitats, as well as the relationship between relative brain size and social evolution.     

The evolution of echolocation in bats

Recent molecular phylogenies have changed our perspective on the evolution of echolocation in bats. These phylogenies suggest that certain bats with sophisticated echolocation (e.g. horseshoe bats) share a common ancestry with non-echolocating bats (e.g. Old World fruit bats). One interpretation of these trees presumes that laryngeal echolocation (calls produced in the larynx) probably evolved in the ancestor of all extant bats. Echolocation might have subsequently been lost in Old World fruit bats, only to evolve secondarily (by tongue clicking) in this family. Remarkable acoustic features such as Doppler shift compensation, whispering echolocation and nasal emission of sound each show multiple convergent origins in bats. The extensive adaptive radiation in echolocation call design is shaped largely by ecology, showing how perceptual challenges imposed by the environment can often override phylogenetic constraints.     

Determinants of echolocation click frequency characteristics in small toothed whales: recent advances from anatomical information

1. The pulse-like clicking sounds made by odontocetes for echolocation (biosonar) can be roughly classified by their frequency characteristics into narrow-band high-frequency (NBHF) clicks with a sharp peak at around 130 kHz and wide-band (WB) clicks with a moderate peak at 30–100 kHz. Structural differences in the sound-producing organs between NBHF species and WB species have not been comprehensively discussed, nor has the formation of NBHF and WB clicks.
2. A review of the sound-producing organs, including the latest findings, could lead to a new hypothesis about the sound production mechanisms. In the current review, data on echolocation click characteristics and on the anatomical structure of the sound-producing organs were compared in 33 species (14 NBHF species and 19 WB species).
3. We review interspecific information on the characteristics of click frequencies and data from computed tomography scans and morphology of the sound-producing organs, accumulated in conventional studies. The morphology of several characteristic structures, such as the melon, the dense connective tissue over the melon (the ‘porpoise capsule’), and the vestibular sacs, was compared interspecifically.
4. Interspecific comparisons suggest that the presence or absence of the porpoise capsule is unlikely to affect echolocation frequency. Folded structures in the vestibular sacs, features that have been overlooked until now, are present in most species with NBHF sound production and not in WB species; the vestibular sacs are therefore likely to be important in determining echolocation click frequency characteristics. The acoustical properties of the shape of the melon and vestibular sacs are important topics for future investigations about the relationship between anatomical structure and sound-producing mechanisms for echolocation clicks.

     

Neurobiology of echolocation in bats

Echolocating bats (sub-order: Microchiroptera) form a highly successful group of animals, comprising approximately 700 species and an estimated 25% of living mammals. Many echolocating bats are nocturnal predators that have evolved a biological sonar system to orient and forage in three-dimensional space. Acoustic signal processing and vocal-motor control are tightly coupled, and successful echolocation depends on the coordination between auditory and motor systems. Indeed, echolocation involves adaptive changes in vocal production patterns, which, in turn, constrain the acoustic information arriving at the bat's ears and the time-scales over which neural computations take place.     

The evolution of flight and echolocation in bats: another leap in the dark

The earliest known complete bats, from the Eocene (49–53 Mya), were already capable of flapping flight and echolocation. In the absence of direct fossil evidence there have been many speculative scenarios advanced to explain the evolution of these behaviours and their distributions in extant bats. Theories assuming chiropteran monophyly have generally presumed the ancestral pre‐bat was nocturnal, arboreal and insectivorous. Following this assumption hypotheses can be divided into the echolocation first, flight first and tandem development hypotheses, all of which assume that flight evolved only once in the lineage. In contrast, the chiropteran diphyly hypothesis suggests that flight evolved twice. Evidence supporting and refuting the different hypotheses are reviewed. It is concluded that there are significant problems attached to all the current models. A novel hypothesis is advanced, which starts from the assumption that bats are monophyletic and the ancestral pre‐bat was arboreal, but diurnal and frugivorous. After the evolution of flight it is suggested that these animals were driven into the nocturnal niche by the evolution of raptorial birds, and different groups evolved either specialised nocturnal vision (megachiropterans) or echolocation (microchiropterans). A block on sensory modality transfer has retained this distribution of perceptual capabilities ever since, despite some Megachiroptera evolving rudimentary echolocation, and the dietary convergence of some Microchiroptera with the Megachiroptera. The new hypothesis overcomes many of the problems identified in previous treatments.     

Parallel evolution of KCNQ4 in echolocating bats

High-frequency hearing is required for echolocating bats to locate, range and identify objects, yet little is known about its molecular basis. The discovery of a high-frequency hearing-related gene, KCNQ4, provides an opportunity to address this question. Here, we obtain the coding regions of KCNQ4 from 15 species of bats, including echolocating bats that have higher frequency hearing and non-echolocating bats that have the same ability as most other species of mammals. The strongly supported protein-tree resolves a monophyletic group containing all bats with higher frequency hearing and this arrangement conflicts with the phylogeny of bats in which these species are paraphyletic. We identify five parallel evolved sites in echolocating bats belonging to both suborders. The evolutionary trajectories of the parallel sites suggest the independent gain of higher frequency hearing ability in echolocating bats. This study highlights the usefulness of convergent or parallel evolutionary studies for finding phenotype-related genes and contributing to the resolution of evolutionary problems.     

Effect of auditory cortical ablation on functioning of the doppler echolocation system in horseshoe bats

The effect of unilateral and bilateral partial and total ablation of the auditory cortex on compensation of Doppler frequency shifts in echosignals was studied in greater horseshoe bats moving in space. The ability of the bats to compensate Doppler surges in the echolocation signal was found to be worsened even after partial ablation of the auditory cortex. Total bilateral ablation led to more marked and irreversible changes in the functioning of the Doppler echolocation system. In this case the degree of compensation in the decorticated animals was only 33% of normal; the return of the frequency of the constant part of the signal to the resting level after movement of the animal ceased was delayed. After total ablation of the auditory cortical projection area definite retrograde degeneration of cells of the medial geniculate body was observed. It is concluded from the results that the auditory cortex in bats plays a direct part in echolocation spatial analysis.A. A. Ukhtomskii Physiological Research Institute, A. A. Zhdanov Leningrad State University. Translated from Neirofiziologiya, Vol. 14, No. 1, pp. 43–50, January–February, 1982.     

Comparative morphology and evolution of the otic region in toothed whales (Cetacea, Mammalia)

The otic region in the skull of archeocetes and odontocetes is compared and interpreted with special emphasis on the morphology and suspension of the ear bones. In archeocetes, the periotic was obviously separate from the mastoid but still integrated within the skull via a long anterior and posterior process. The rotation of the cochlear part of the periotic was already obvious. The tympanic bone was attached to a decreasing number of neighboring elements, with the periotic becoming more and more important in the later archeocetes. The accessory air sacs of the tympanic cavity had invaded some of the adjacent skeletal elements and attained a moderate-to-remarkable extension. In the evolution of the odontocetes, the periotic and tympanic were successively uncoupled from the skull and combined to a new morphological and functional unit (tympanoperiotic complex). This uncoupling was mainly achieved by shortening the periotical processes and simultaneously extending the tympanic air sacs. For functional reasons, however, the periotic (posterior process) stayed in immediate contact with the mastoid, the latter remaining in the lateral wall of skull. In advanced marine dolphins, the bony sheaths of the accessory air sacs are largely reduced, presumably because of volume fluctuations in the tympanic cavity during diving. The perfect uncoupling of the ear bones from the skull obviously was an essential prerequisite for directional hearing, for effective ultrasound orientation and communication, and finally, for the striking development of the dolphin brain.     

A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales

Extant baleen whales (Cetacea, Mysticeti) are all large filter-feeding marine mammals that lack teeth as adults, instead possessing baleen, and feed on small marine animals in bulk. The early evolution of these superlative mammals, and their unique feeding method, has hitherto remained enigmatic. Here, I report a new toothed mysticete from the Late Oligocene of Australia that is more archaic than any previously described. Unlike all other mysticetes, this new whale was small, had enormous eyes and lacked derived adaptations for bulk filter-feeding. Several morphological features suggest that this mysticete was a macrophagous predator, being convergent on some Mesozoic marine reptiles and the extant leopard seal (Hydrurga leptonyx). It thus refutes the notions that all stem mysticetes were filter-feeders, and that the origins and initial radiation of mysticetes was linked to the evolution of filter-feeding. Mysticetes evidently radiated into a variety of disparate forms and feeding ecologies before the evolution of baleen or filter-feeding. The phylogenetic context of the new whale indicates that basal mysticetes were macrophagous predators that did not employ filter-feeding or echolocation, and that the evolution of characters associated with bulk filter-feeding was gradual.     

Phenotypic traits evolution and morphological traits associated with echolocation calls in cryptic horseshoe bats (Rhinolophidae)

Bats provide an excellent casestudy for studying evolution due to their remarkable flight and echolocation capabilities. In this study, we sought to understand the phenotypic evolution of key traits in Rhinolophidae (horseshoe bats) using phylogenetic comparative methods. We aimed to test the phylogenetic signals of traits, and evaluated the best-fit evolutionary models given the data for each trait considering different traits may evolve under different models (i.e., Brownian Motion [BM], Ornstein-Uhlenbeck [OU], and Early Burst [EB]) and reconstruct ancestral character states. We examined how phenotypic characters are associated with echolocation calls and minimum detectable prey size. We measured 34 traits of 10 Asian rhinolophids species (187 individuals). We found that the majority of traits showed a high phylogenetic signal based on Blomberg′s K and Pagel′s λ, but each trait may evolve under different evolutionary models. Sella traits were shown to evolve under stabilizing selection based on OU models, indicating sella traits have the tendency to move forward along the branches toward some medial value in equilibrium. Our findings highlight the importance of sella characters in association with echolocation call emissions in Rhinolophidae, as calls are important for spatial cognition and also influence dietary preferences. Minimum detectable prey size in Rhinolophidae was associated with call frequency, bandwidth, call duration, wingspan, and wing surface area. Ultimately, understanding trait evolution requires sensitivity due to the differential selective pressures which may apply to different characteristics.     

Adaptive vocal behavior drives perception by echolocation in bats

Echolocation operates through adaptive sensorimotor systems that collectively enable the bat to localize and track sonar objects as it flies. The features of sonar signals used by a bat to probe its surroundings determine the information available to its acoustic imaging system. In turn, the bat's perception of a complex scene guides its active adjustments in the features of subsequent sonar vocalizations. Here, we propose that the bat's active vocal-motor behaviors play directly into its representation of a dynamic auditory scene.     

Embryonic evidence uncovers convergent origins of laryngeal echolocation in bats

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