Yin and yang

There are six distinct and presumably ancient microbat lineages, each of which has evolved its own version of sonar, based on ultrasonic vocalisation and echolocation. Fruit bats, with the singular exception of members of the genus Rousettus, do not echolocate.

Rousettus uses echolocation to find its way around in the dark caves where it lives but it employs audible tongue clicks, not ultrasonic squeaks. Pettigrew argues that Rousettus evolved echolocation relatively recently, and independently of microbats.

On comparative DNA evidence, molecular taxonomists have proposed a yin-yang scheme that groups all bats within two suborders: Yinpterochiroptera, which includes all fruit bats and members of the rhinolophoid superfamily of microbats, and the Yangochiroptera, which includes all other echolocating microbat lineages.

Ultrasonic-echolocating Yinpterochiroptera - excluding fruit bats - are mainly constant-frequency, nasal emitters that can compensate for Doppler-shifted echoes as their flight speed varies.

In contrast, most Yangochiroptera employ orally emitted, ultrasonic, frequency modulated vocalisation.

But there are many exceptions. Sonar adaptations like nasal emission and whispering echolocation, compensation for Doppler shifted echoes, and passive listening to localise prey, have clearly evolved multiple times in phylogenetically distant groups.

The ancestor of microbats - a glider - diverged around 80 million years ago from other major mammalian lineages in the super-order Laurasiatheria, which includes hedgehogs, moles, shrews, cetaceans (whales, porpoises and dolphins), ungulates like pigs, hippopotamus, camels, horses and ruminants, pangolins and carnivores.

The major microbat lineages arose during a burst of evolutionary radiation in the Eocene, which may have been driven by the development of ultrasonic echolocation.

The announcement in February of the discovery of a primitive fossil microbat in 52-million year old early Eocene rocks in Wyoming's Green River Formation allows the evolutionary radiation of echolocating microbats to be accurately dated.

Onychonycteris finneyi bears a strong physical resemblance to latter-day microbats, except that it has claws on all five fingers, compared with only one or two in modern bats. It also has longer hind legs, and shorter forearms, suggesting it was formerly a climber that dangled beneath branches, like sloths.

But O. finneyi lacked the ear anatomy to detect ultrasound -- it may have been a daytime hunter, that relied on eyesight to hunt insects on the wing. Icaronycteris, the earliest microbat previously known from the fossil record, came from the same formation. Just 2 million years after O. finneyi, it was hunting with ultrasonic sonar.

Li et al observe that echolocation places extreme demands on bats' sensory and motor systems. A hunting microbat can emit up to 200 ultrasonic chirps per second, interpret the returning echoes, and make appropriate motor responses, including changes in flight direction and speed, all within a few milliseconds.

These demands have placed extreme selection pressure on the gene that coordinates it all - FOXP2 - that is apparent in the highest level of sequence variation in any mammalian order. Interestingly, Li et al observe that bats are among only few groups of vertebrates that exhibit vocal learning, a likely precursor to language.

The two most variable exons are exon 7 - the three human mutations also occur within this exon - and exon 17.

Only one lineage of bats has no variation in exon 17: Professor Pettigrew's "flying primates", the fruit bats. Like primates, they share the archetypal mammalian version of exon 17.