Rich acoustic landscapes dominated the Mesozoic

The history of life on earth has captivated the human imagination for millennia. We want to know how ancient animals lived and died, and that can help us understand where we came from, and how the world might yet change. Fossils capture snapshots of organisms and traces of their activities, but only rarely do they reflect interactions between animals, and between animals and their environment (1). Yet, ecological interactions—from predator-prey dynamics, to mutualistic and consumer relationships—are key drivers of macroevolutionary processes from lineage diversification to evolutionary innovation (2). Similarly, social interactions—like communication between individuals of the same species—also play critical roles in animals’ lives with wide-reaching evolutionary consequences (3). Reconstructing the behavior of ancient animals is therefore key to understanding Earth’s history; and, the fossilized evidence of complex insect behaviors described by Xu et al. in PNAS (4) paints a richer picture of what life on earth was like in the Mesozoic and how life evolved to what we see today (Fig. 1).

Fig. 1.

This image from the supplemental material of Xu et al. in PNAS (4), depicts a scene rich with singing katydids.

Xu et al. describe complex behaviors (sound production) and sensory organs (ears) involved in acoustic communication and hearing (4). Their work has implications for the types of social and ecological interactions that occurred between Mesozoic katydids and the other animals in their environment and the concurrent evolution of acoustic sensory systems. Xu et al. pulled together a large assembly of beautifully preserved katydid specimens dating back to the late Triassic, and used modern analogs to calculate the pitch of their broadcasted songs (4). In addition to documenting that song was already widespread and very diverse in the Mesozoic, Xu et al. also document the earliest known tympanic ear in insects and show that this complex sensory structure was widespread (4). Prior to Xu et al.’s paper in PNAS, evidence for insect acoustic communication in the Mesozoic was constrained to a single specimen, dating back to 165 million years ago (5). Furthermore, there are very few examples in the entire fossil record that document any type of communication in animals; only a few examples exist for insects; and even fewer fossils document acoustic communication (1). Thus, Xu et al.’s description of a wide diversity of acoustic communication (4)—in conjunction with a recent paper on the origins of vertebrate acoustic communication (6)—significantly expands our knowledge of the acoustic environment in the Mesozoic. In fact, Xu et al. establish that acoustic communication in insects evolved at least 100 million years earlier than previously thought (4).

It is clear from Xu et al. (4), that ancient katydids and their close relatives produced a cacophony of sound that filled the night air, much as they do in in the modern day. What exactly does this reveal about life on earth during the Mesozoic? To answer this question, one must understand the dynamics of acoustic communication and the complex morphological and sensory adaptations that facilitate it. Acoustic communication involves the transfer of information from one individual to another through sound waves. While sound can travel through a variety of substrate types—including air, below water, as water surface ripples, and through the ground and other solid substrates like plants—we will refer to it here as sound traveling as pressure waves through the air. Importantly, airborne acoustic communication allows for long-distance information exchange even when obstructions are in place or light levels are low; for example, a nocturnal lifestyle was a major determinant of the evolution of vertebrate acoustic communication (6).

Xu et al. establish that acoustic communication in insects evolved at least 100 million years earlier than previously thought.

Long-distance acoustic communication brought many advantages for Mesozoic katydids, including locating and assessing rivals or mates from a safe distance under varying light conditions. To be able to take advantage of long-distance acoustic communication, insects need to both encode and extract relevant information like the location and species identity of mates and rivals. For modern insects—and now we know also for Mesozoic insects (4)—variation in acoustic signals across species is quite common, allowing for females and rival males to identify songs relevant to them. When multiple animals living together evolve diverse songs as demonstrated by Xu et al. (4), the phenomenon is referred to as acoustic niche partitioning. Each species takes up a distinct band of sound in the sound spectrum, allowing for multiple acoustic animals and multiple ecologically similar organisms—like many species of Mesozoic katydids—to coexist. Interestingly, the study by Xu et al. (4) parallels advances in the field of bioacoustics (the study of biologically relevant sound) in its rapid expansion to encompass entire acoustic scenes rather than focusing on single species. Bioacousticians are then using these auditory scenes to study ecosystem health and disturbance (e.g., ref. 7). Thus, it is possible that a more thorough understanding of the acoustic landscape from the fossil record may even provide insight into entire ancient ecosystems.

In addition to encoding information acoustically, intended receivers (e.g., female katydids) must be able to capture and process sounds. Out of water, the impedance mismatch between air and animal tissue requires specialized sound detection organs, and multiple insect clades have independently come up with the same solution to this challenge: tympanic ears. In fact, land vertebrates have also converged on similar tympanic morphologies (8). Tympanal organs in insects have three primary components: a tympanal membrane (i.e., eardrum), an air-filled cavity behind the tympanum, and a chordotonal sensory organ that encodes the received sound into neuronal firings. There are 18 independent origins of tympanal organs in at least 7 orders of insects (9, 10). These occur most often in flying insects that require advanced tracheal systems to power flight, where the tracheal system is coopted into the eardrum (10). In katydids, the cordotonal organ is derived from a proprioceptive organ in the foreleg (11), originally designed to detect mechanical disturbance like vibrations traveling through plants. The proprioceptive organs were also likely used in acoustic communication far before airborne acoustic communication arose because the vast majority of modern “acoustic” insects use either solely substrate-borne vibrations (sound traveling as vibrations through solid objects, like plant stems and leaves), or substrate-borne vibrations in conjunction with airborne sound (12).

Sound production mechanisms are more often preserved than sound perception structures in insects (13). Even in modern insects, finding evidence of hearing is extraordinarily challenging (9). Thus, Xu et al.’s (4) examination of numerous preserved ears is truly incredible. Furthermore, the discovery of the earliest known example of the modern tympanal insect ear has significance beyond the obvious. The evolution of tympanic ears would be accompanied by changes in the central nervous system for processing high-frequency sound and directional cues (14). Fossilized ears therefore provide insight into not only behavior and communication systems, but also the evolution of complex nervous systems.

Hearing is used for more than just communication in animals. The detection of sound is critical for detecting and avoiding predators. While surprisingly little is known about how insect hearing is used to avoid predators beyond the detection and evasion of bats (15), hearing in insects has evolved more often than acoustic communication, pointing to the importance of sound detection for predator avoidance (10). In Orthopterans (including katydids) and Hemipterans (true bugs), ears and sound production systems have evolved relatively closely together in time (10), indicating the importance in Mesozoic katydid ears in communication in addition to any antipredator functions.

Unfortunately for singing insects in the Mesozoic, broadcasting song to potential rivals and mates also made them susceptible to acoustically orienting predators. Prior to the evolution of airborne acoustic songs, most biologically relevant sound was clustered in the low frequencies, as it is today (16). Phylogenetic reconstructions indicate that the vertebrate tympanic ear evolved multiple times in the early Triassic, allowing for better hearing than atympanic ears, particularly at higher frequencies (8). These tympanic organs are precisely the types of ears that would allow land vertebrates to successfully eavesdrop on katydid song. Additionally, the higher frequency songs described by Xu et al., likely also put new selection pressures on tetrapods to have the central nervous system processing capable of detecting high-frequency sound and discern directionality (14). The origin for the upper part of modern human’s range of hearing (20 to 20,000 Hz) may therefore have origins dating back to the acoustic landscape created by Triassic katydids!

Xu et al. have uncovered a treasure trove of fossilized specimens documenting acoustic communication from the Mesozoic (4), a remarkable find given only the most fortuitously captured fossils allow us to examine behavior (17). Additionally, only exceptionally well-preserved fossils allow us to examine the behaviors involved in acoustic communication, which involves fine-scale structures to produce and perceive sound. However, despite the rarity of preserving communication systems, the numerous fossil specimens described by Xu et al. suggest that the fossilization of acoustic communication in insects may be more common than originally thought. Thus, this paper calls attention to the need for increased collaboration between paleobiologists and animal behaviorists (sensu (17)).

Behaviors underlying social and ecological interactions are rarely captured in the fossil record, are often inferred from trace fossils (e.g., herbivory on plants or tracks in the ground) (1), and most commonly involve single-case studies. In contrast, Xu et al. (4) do more than describe the earliest incidence of modern tympanic ears in insects and song diversity of Mesozoic katydids. They additionally depict a world rich with a wide variety of songs that shaped social and ecological interactions, and insect and vertebrate hearing and nervous systems. This important scientific discovery further provides an acoustic avenue to imagine ancient life on earth (Fig. 1).