(Embargo lifts at 5 a.m. Pacific Time, July 31, 2018)

Doctoral candidate Philipp Brand and his colleagues at the University of California, Davis, had just finished compiling the genome or complete set of genetic material of the firebrat--a tiny wingless, nocturnal insect found throughout much of the world--when something surprised him.

There they were--odorant receptor genes, the scent-detecting genes thought to have evolved with winged insects more than 400 million years ago. But this groundbreaking discovery indicates they evolved millions of years earlier.

The sensory gene is considered one of an insect's most important genes, crucial to foraging, mating and avoiding predators.

“It was interesting because a paper published in 2014 claimed that ORs evolved with winged flight and were thus absent in ancestrally wingless (Apterygota) insects,” said Brand, a member of the Population Biology Graduate Group who researches the evolution of olfactory/odorant receptor genes in orchid bees. “Since firebrats are apterygote, we now had proof that this gene family is more ancient than previously thought.”

“A week or so after our discovery, a paper coming to the same conclusion but with indirect evidence was posted on the preprint server bioRxiv.” Brand related. That was the sole work of Professor Hugh Robertson of the Department of Entomology, University of Illinois at Urbana Champaign, who specializes in molecular biology and genomics.

Brand proposed that they merge their datasets and write a comprehensive paper of higher impact rather than two independent papers. It was a “go.”

The collaborative result: “The Origin of the Odorant Receptor Gene Family in Insects,” a newly published paper by a seven-member team from UC Davis, University of Illinois and the University of Tennessee, in the open-access journal eLife, which prints promising research in the life and medical sciences. The article is online at  https://doi.org/10.7554/eLife.38340

 “Our finding that the odorant receptor gene family evolved at the evolutionary base of the insects makes it a major evolutionary novelty that presumably contributed to the adaptation of early insects to terrestrial living,” Robertson said.

 Said Brand: “Odorant receptors are the largest insect gene family underlying the sense of smell. ORs are thus crucial in the majority of behaviors that involve the sense of smell including foraging, reproduction, and detection of predators.” The cell membranes of odorant receptor neurons are key to detecting scents. In insects, the ORs are usually found in the antennae or mouthparts.

In an effort to identify the origin of the insect OR gene family and the ancestral OR co-receptor (Orco), the team investigated the genome sequences of species belonging to multiple insect and other terrestrial hexapod orders, specifically Collembola (springtails), Diplura (two-pronged bristletails), Archaeognatha (jumping bristletails), Zygentoma (silverfish and firebrats), Odonata (damselflies and dragonflies), and Ephemeroptera (mayflies). A hexapod is a six-legged arthropod named for its most distinctive feature: a consolidated thorax with three pairs of legs (six legs). Most other arthropods have more than three pairs of legs.

In their abstract, the authors wrote that “The origin of the insect odorant receptor (OR) gene family has been hypothesized to have coincided with the evolution of terrestriality in insects. (Christine) Missbach et al. (2014) suggested that ORs instead evolved with an ancestral OR co-receptor (Orco) after the origin of terrestriality and the OR/Orco system is an adaptation to winged flight in insects. We investigated genomes of the Collembola, Diplura, Archaeognatha,

Zygentoma, Odonata, and Ephemeroptera, and find ORs present in all insect genomes butabsent from lineages predating the evolution of insects. Orco is absent only in the ancestrally wingless insect lineage Archaeognatha. Our new genome sequence of the zygentoman firebrat, Thermobia domestica, reveals a full OR/Orco system. We conclude that ORs evolved before winged flight, perhaps as an adaptation to terrestriality, representing a key evolutionary novelty in the ancestor of all insects, and hence a molecular synapomorphy for the Class Insecta.”

Synapomorphy is defined as a characteristic present in an ancestral species and shared exclusively by its evolutionary descendants.

The research is a UC Davis cross-departmental collaboration involving associate professor Brian Johnson of the Davis Department of Entomology and Nematology, Wei Lin of the Johnson lab and a member of the Entomology Graduate Group; and Brand, who studies with major professor Santiago Ramirez of the Department of Evolution and Ecology.

“A recurring theme in the field of genomics is that incomplete sampling of the relevant taxa often leads to premature conclusions,” said Johnson. “Our work on ORs is a good example of this.” Johnson studies the genetics, behavior, evolution, and health of honey bees. His lab currently focuses on the evolution and genetic basis of social behavior using comparative and functional genomics.”

The seven-member team, in addition to the UC Davis and University of Illinois scientists, included a trio from the University of Tennessee: Ratnasri Pothula, William Klingeman, and Juan Luis Jurat-Fuentes.

Brand recalled that he detected the multiple odorant receptor genes in the firebrat genome in late January or early February. “I was working at home after my normal work day, because this genome work I did with Brian was a side project for me—he knew of my interest in genomics and offered me the opportunity to collaborate on his lab's ongoing projects.” 

Brand expects to receive his doctorate from UC Davis in the spring of 2019. A native of Germany and a former research scientist at Ruhr-University, Bochum, he received his master's degree in genetics and evolutionary biology in 2013 from Ruhr-University, and his bachelor's degree in biology in 2010 from Heinrich-Heine University, Düsseldorf, Germany.

Earlier this year Brand won the Genome Biology and Evolution (GBE) Best Graduate Paper Award for “The Evolutionary Dynamics of the Odorant Receptor Gene Family in Corbiculate Bees,” published in GBE in 2017 (https://www.ncbi.nlm.nih.gov/pubmed/28854688). Corbiculate refers to pollen-basket bees such as orchid bees, bumble bees, honey bees and stingless bees. His research also won him the Best Graduate Student Poster Award at the 2017 UC Davis Bee Symposium.

Winged insects first appeared on earth 406 million years ago, according to research published in a 2014 edition Science by molecular biodiversity researcher Bernhard Misof, a professor at the University of Bonn, Germany.

Fossil records indicate that hexapods diverged from crustaceans 410 to 510 million years ago, according to Misof. “At this time in geological history, land masses were dotted with shallow inland seas, and plant life (mostly algae and bryophytes) was largely restricted to coastal habitats and other sites where water was readily available,” according to a North Carolina State University's Department of Entomology website. “The oldest hexapod fossils are found in rocks of the late Devonian period. These rocks also contain numerous other terrestrial arthropods (mites, spiders, centipedes, scorpions, etc.) suggesting that a major radiation of terrestrial life-forms must have occurred during the Ordovician or Silurian period.”

The first known fossil record of Apterygota insects, which include firebrats, silverfish and jumping bristletails—dates back to the Devonian period, which began 417 years ago.

The firebrat, found throughout the world under rocks and leaf litter, is an indoor pest of dog food, stored foods, fabric and book bindings. It is commonly found in high-humidity environments such as bakeries and boiler rooms.

According to the UC Statewide Integrated Pest Management Program (UC IPM), both firebrats and their cousin silverfish “have enzymes in their gut that digest cellulose, and they choose bookcases, closets, and places where books, clothing, starch, or dry foods are available. Silverfish and firebrats are nocturnal and hide during the day. If the object they are hiding beneath is moved, they will dart toward another secluded place. They come out at night to seek food and water. Both insects prefer dry food such as cereals, flour, pasta, and pet food; paper with glue or paste; sizing in paper including wallpaper; book bindings; and starch in clothing. Household dust and debris, dead insects, and certain fungi also are important sources of food. However, they can live for several months without nourishment.”

“Large numbers of these insects can invade new homes from surrounding wild areas, especially as these areas dry out during the summer,” the UC IPM website says. “They also can come in on lumber, wallboard, and similar products. Freshly laid concrete and green lumber supply humidity, while wallpaper paste provides food.”

Resources:
eLife:  https://doi.org/10.7554/eLife.38340
UC IPM Pest Note on Firebrat: http://ipm.ucanr.edu/PMG/PESTNOTES/pn7475.html
Information on hexapods: https://genent.cals.ncsu.edu/bug-bytes/hexapods/
Philipp Brand website: https://evolvingors.wordpress.com

Contacts:
Philipp Brand: pbrand@ucdavis.edu
Brian Johnson: brnjohnson@ucdavis.edu
Hugh Robertson: hughrobe@uiuc.edu