The eyes have it

It was the structure of the fruit bat eye, and the neural circuitry of the brain's visual regions, that originally alerted Jack Pettigrew to the remarkable possibility that fruit bats share an ancestor with primates, not microbats, and that mammals must thus have evolved flapping flight twice.

Both colugos and fruit bats share with primates a distinctive eye structure in which the nerves from the light-sensing retina at the rear of the eye project forward before turning back through a central gap in the retina to connect to the brain.

As a result, the primate eye has a small blind spot at the centre of its visual field. Behind the eyes, the optic nerves connect to the brain via a structure called the lateral geniculate nucleus (LGN). In the primate, fruit bat and colugo, the LGN has six interleaved layers of nerves - three from each eye - that integrate the separate images from each eye.

Megabats devote more of their neocortex - the outer "modern" layer of the brain where sensory input is processed - to vision than any other mammal. The corresponding region in microbats is relatively tiny, and the auditory region correspondingly large, as might be expected for a mammal that lives in a world dominated by sound.

Microbats leave their young at home, in communal nurseries, while foraging. Megabats, like primates, carry their young with them until they become too heavy. Newborn microbats do not open their eyes for several weeks; baby megabats open their eyes at birth.

Chromosome counts in the 17 different families of microbats vary widely, suggesting the lineages are ancient. All megabats have the same chromosome count, indicating a more recent origin.

Microbat and megabat sperm are very different, and sperm structure is a basic indicator of relationships between species.

Megabats and microbats carry external parasites, including fleas and flies, but they represent different families.

Blood serum proteins, including haemoglobin, clearly link megabats with primates, and indicate a distant relationship with microbats. Alpha-crystallin, the clear, crystalline protein that forms the lens of the eye, tells a similar tale.

Pettigrew says when fruit bats and colugos defecate, they reverse position and dangle head-up by their hooked wing "thumbs". The colugo shares this demure posture, hanging by its thumbs during defecation. In contrast, microbats dangle by their back legs and arch their backs to avoid soiling their fur.

Microbats take their prey on the wing, while other species hover on the wing to sip nectar from flowers. Fruit bats land in trees to forage for fruit, and despite their wings, are agile climbers, moving like lemurs, according to Pettigrew.

Fruit bats have mammary glands on the chest, like primates, not on the abdomen, like most mammals.

Male megabats have a soft, pendulous penis with a prominent glans, like primates. Microbats have a bony penis, sans glans.

And last August, Chinese researchers reported an almost definitive clue linking fruit bats to primates: fruit bats have a menstrual cycle - a universal trait in primates, but very rare among the world's other, 4000-odd mammals.