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Sound-making, hearing mechanisms in crickets date back 300 million years

by Adam Russell, Texas A&M AgriLife Marketing and Communications

Songs produced by crickets, katydids, grasshoppers and other orthopteran insects are hundreds of millions of years in the making, according to a Texas A&M AgriLife Research scientist’s research published in Nature Communications.

Hojun Song, Ph.D., AgriLife Research entomologist and associate professor in the Department of Entomology at Texas A&M University, Bryan-College Station, said there have been many changes to the way insects within the Orthoptera order hear and create sounds, but the lineage of these songs dates back around 350 million years.

“We may take it for granted when we hear crickets and katydids, but these insects are involved in very complex acts of communication,” he said. “Just like we use vocal cords and ears to relay messages in acoustic communication, these insects are engaged in a communication that is some of the oldest on Earth.”

The research publication “Phylogenomic analysis sheds light on the evolutionary pathways towards acoustic communication in Orthoptera” shows that the lineages of Orthoptera were communicating to find mates, avoid predators and navigate throughout 350 million years of diversification. By investigating these ancient communication methods, humans can better understand how we ourselves communicate, Song said.

The research was a five-year project funded by the National Science Foundation and the 1KITE, 1K Insect Transcriptome Evolution project, a large international consortium aiming to study the transcriptomes, or the entirety of expressed genes, of more than 1,000 insect species from all recognized insect orders. The publication included work from 12 other scientists from around the globe and is accessible to anyone.

“We discovered a great deal, but there is a great deal that is yet to be discovered about acoustic communication in Orthoptera,” Song said. “But the practical applications of our study are also exciting because it is possible to develop novel tools, such as hearing aid devices, modeled after these ancient mechanisms used for acoustic communication.”

Why crickets and katydids?

In terms of animal sounds, insects are the most diverse communicators on the planet, Song said. There are thousands of mammalian and avian species that communicate acoustically for mating, defense and navigation, but there are tens of thousands of insect species that make and hear sounds.

Song and the other researchers approached the project by poring over extensive literature and by using phylogeny, which refers to the evolutionary relationships among organisms. They also collected DNA- and RNA-quality samples of a wide range of Orthoptera species from around the globe and viewed curated species collections and fossil records.

The researchers deduced relationships and built a phylogeny based on DNA sampling and gene sequencing methods, including transcriptome analysis, which have improved exponentially over the past decade.

“A few data points can give a glimpse of the evolutionary relationships, but the amount of data we can generate now can give us a very clear view of the relationships among those species we sampled,” he said. “The transcriptome analysis helped us build a reliable family tree.”

The Orthoptera order encompasses about 28,000 known species, and around 16,000 of them communicate acoustically, Song said. These insects use various specialized mechanisms on their wings or legs and abdomens to create and hear sounds.

Some crickets’ wings have microscopic teeth on the underside that look like a file. When rubbed by a scraping mechanism on the other wing, the “teeth” emit the tell-tale chirp. Some grasshoppers scrape their legs with their wings. Some species of katydids communicate at frequencies at the ultrasound level, which is too high for the human ear to perceive.

Hearing mechanisms also vary from species to species, Song said. Crickets and katydids have ears on their legs. Grasshoppers have ears on their abdomen.

The authors sampled 239 species of Orthoptera for the analyses. The specimens exhibited a wide range of characteristics representing the diversity of acoustic communication within the Orthoptera order.

“There are 16,000 species that communicate acoustically, so we had to select species that covered a wide enough range of characteristics to build a robust evolutionary relationship phylogeny that investigated the use of hearing and sound producing mechanisms,” he said.

After scientists established relationships among the species, they used fossil data to calibrate the phylogeny and determine how old the lineages were, Song said. A paleontologist reviewed millions-year-old fossils of grasshoppers, katydids and crickets to create a “time tree” representing how and when the different insect lineages diverged within the Orthoptera order.

Some of the fossils that the paleontologist reviewed included a cricket’s wing from the Triassic Period, 251 million-199 million years ago. The wing displays the same scraper and teeth that crickets currently use to create sound, Song said.

“What we found was that crickets were using the same mechanism to communicate as they do today,” he said. “So, if we had a time machine, we could go back 300 million years and hear a cricket song that is the same or very similar to what we hear today.”

Song and researchers used that information as a calibration point to go back even further. They estimated, based on 272-million-year-old fossil evidence, that the crown-Orthoptera species appeared during the late Carboniferous period, around 350 million years ago.

Evolution of hearing and sound production

Song said some species within Orthoptera that appeared later likely evolved their communication to stand out in an increasingly noisy environment. They developed advanced sound tempos, patterns and frequencies to stand out among other species to attract mates.

Communication became more complicated as animal life exploded during the Jurassic and Cretaceous periods, Song said.

“There were more species entering the soundscape, and it was becoming saturated, so species probably had to find their narrow niche to communicate,” he said. “Their song had to stand out to mates, so they specialized, but they also had to avoid predators that were homing in via sound.”

Scientists determined very different divergences within two orthopteran suborders – Caelifera and Ensifera, Song said.

Within Ensifera, which includes crickets, katydids, mole crickets and grigs, sound-producing mechanisms and ears likely co-evolved from about 300 million years ago, Song said.

Within Caelifera, which includes grasshoppers, the time tree shows most ancient grasshoppers evolved hearing mechanisms around 60 million years ago, prior to the evolution of sound production. Their hearing mechanism – the abdominal tympana – led to a great divergence in Orthoptera species.

“They may have developed hearing to avoid predators or to modulate their flight,” he said. “But the ability to hear opened up the possibility to communicate. Those evolutionary changes led to many divergences over millions of years.”

What’s next?

Song has recently received another round of funding from National Science Foundation to use more species and more sophisticated technology. His international team, now including collaborators from the U.S., the U.K., France and South Korea, will increase the number of species sequenced to 1,600 and apply biomechanics and biophysics to investigate how the functions of stridulatory wings and tympanal ears have evolved.

Despite many studies, the evolution of acoustic communication is still an open field to scientists, Song said. The research has major implications for insect species’ sustainability in the changing environment and acoustic communication throughout the animal kingdom, including humans.

“Insects, like many species, are adapted to their environment,” he said. “Urbanization is changing the soundscape these insects communicate in. If we can understand these mechanisms and how Orthoptera make sound and hear, we will know more about how we hear and maybe develop novel technology that improves the acoustic environment and acoustic communication for all communicating life, from Orthoptera species to humans.”

Multi-university collaboration funded by a 5-year, $12.5 million grant

by Olga Kuchment, Texas A&M AgriLife Marketing and Communications

Locusts have a reputation of biblical proportions. Certain species of grasshoppers that are typically solitary and harmless can suddenly swarm and consume entire crops, including plants that support livestock. Large swarms can destroy livelihoods for farmers and entire communities’ food supply.

That is why researchers from Texas A&M AgriLife, Baylor College of Medicine, Arizona State University, Washington University in St. Louis and University of California, Davis, have created the Behavioral Plasticity Research Institute, BPRI.

The institute will work to understand the mechanisms behind locust swarms and migration, and then use this knowledge to develop effective methods to limit the destruction the swarms can leave behind.

The cross-institutional, multi-disciplinary effort is led by Hojun Song, Ph.D., associate professor, and Spencer Behmer, Ph.D., professor, both in the Texas A&M College of Agriculture and Life Sciences Department of Entomology; Fabrizio Gabbiani, Ph.D., professor of neuroscience, and Herman Dierick, M.D., associate professor of molecular and human genetics, both at Baylor; and Arianne Cease, Ph.D., associate professor of sustainability and director of the Global Locust Initiative at Arizona State University.

The team with wide-ranging expertise also includes Gregory Sword, Ph.D., professor, Texas A&M Department of Entomology; Erez Lieberman, Ph.D., assistant professor, and Chenghang Zong, Ph.D., assistant professor, both at Baylor; Rick Overson, Ph.D., senior scientist, Arizona State; Stephen Richards, Ph.D., project scientist, Earth BioGenome Project, UC Davis; and Barani Raman, Ph.D., professor, Washington University.

The Behavioral Plasticity Research Institute

A $12.5 million, five-year National Science Foundation grant provides funding for the BPRI. The institute is one of four inaugural Biology Integration Institutes established by the NSF this year to work on broad problems in biology.

“Using cutting-edge technologies in research projects spanning from molecules to landscapes, the BPRI will greatly enhance our understanding of how grasshoppers transform into locusts – a phenomenon called locust phase polyphenism – and develop innovative solutions to manage locust plagues,” Gabbiani said. “With a commitment to improving diversity, inclusion and equity, the institute will train the next generation of integrative biologists who can efficiently navigate across disciplines to reach this goal.”

The institute will communicate groundbreaking research to the general public and the scientific community. By partnering with the Global Locust Initiative hosted at Arizona State, the institute plans to translate its scientific findings to real-world management with a goal of improving global food system sustainability.

Nature vs. nurture

The phenomenon BPRI will study, locust phase polyphenism, is a prime example of how distinct phenotypes can arise from environmental and other cues, rather than only genetic information. In the case of grasshopper species that are considered to be locusts, typically harmless insects can change their behavior in response to certain environmental and sensory cues to become a cohesive swarm.

The changes locusts undergo belong to a broad scientific concept known as phenotypic plasticity, the ability of organisms to change in response to their environment. Phenotypic plasticity is common in nature. But, to fully understand its mechanisms, maintenance and evolution, biological integration is needed, Song said. This work also illuminates how gene expression patterns and epigenetic regulation are linked to shifts in behavior, physiology and ecology that result in outbreaks, collective movement and mass migration.

So, the team expects this work to eventually lend itself to more than just insects. The information learned will help to understand how environment influences genetic makeup to shape behavior across all animals.

Global impact, local solutions

“Currently, when locusts outbreak, they can affect one in 10 people globally,” Behmer said. “The impact and the benefits to society that might come from this institute are pretty enormous.”

To better understand the scope of locusts’ impact, one must consider the situation of places affected by swarms, Sword said.

“When we have disasters in developed countries, we have mechanisms in place to get people support and relief they need,” Sword said. “But in a country dependent on small-holder subsistence agricultural operations, a locust swarm can literally take away a family’s entire source of income and food for the year.”

Hence, to gain a fuller understanding of the problem and provide individualized solutions, the institute will involve people with diverse backgrounds.

“Every step of the way, we will ask the question of whether we are being inclusive and hearing all the perspectives,” Song said. “We need to work across subdisciplines and try to get at the big picture rather than focusing on little slices. I believe that by bringing all these people together, within the next five or 10 years, we can make amazing changes.”

Ten integrative research projects

Researchers with the BPRI plan to carry out 10 integrative research activities. The projects will use three locust and three non-swarming grasshopper species with varying degrees of plasticity. The researchers will work with genomes, tissue-specific and time-resolved transcriptomes and epigenomes, as well as CRISPR/Cas9 and reverse genetics tools to understand the functional genetics of locust phase polyphenism, all considered within an evolutionary framework.

“We’ll be studying the factors that nudge individual locusts to join a larger group and the changes that follow,” Raman said. “Given the reports of massive, destructive locust swarms in many African and Asian countries this year, this is indeed a timely investigation of a well-reported, but not yet fully understood phenomenon.”

In essence, the institute will aim to solve problems humans have faced for thousands of years due to locusts, Song said.

“We’ve had the locust problem for millennia,” Song said. “But, we still struggle to control these pests. I believe that the discoveries made through the BPRI will fundamentally transform our understanding of why and how locusts swarm, which will ultimately translate into sustainable management practices.”