The Origin and Evolution of Bats part 3

Earlier here, here and here we looked at the origin and evolution of bats. Now let’s add a few more pieces to the puzzle to make the transitions more complete, more logical and more gradual.

The bat flight stroke
(Fig. 1) is similar to that of birds during takeoff, when the airspeed is minimal. So, there is less reliance here on Bernoulli’s principle and more Newton’s third law as the bat wing scoops up and pushes down a mass of air with each downstroke. The incredible ability of bats to ‘turn on a dime’ is due to their ability to greatly modify their wings in flight, push a volume of air in any direction, and to play the mass of their own wings against the remaining 80% to push maneuvers birds would never try. This includes the ability of bats to invert themselves at low airspeed in order to cling to ceilings and perform an upside-down, two-point landing.

In bats the wing stroke 
cycles from extension and maximum wing area (on the downstroke) to flexion with minimum wing area (on the upstroke). On some bats the wing tips ventrally touch one another during the flight stroke, but on this Myotis specimen (Fig. 1) the wing tips graze the torso. This sort of flight stroke appears to have evolved from a prey gathering stroke when the much smaller forelimbs were simply enlarged webbed hands (Fig. 5).

Bats were not always so incredibly gifted in flight.
Obviously there were millions of transitional generations that evolved from quadrupedal arboreal forms in the Late Cretaceous before bats became such supreme aerialists in the Early Eocene.

The question is:
what sort of behavior led to this sort of flight stroke on non-flying bat ancestors with small unwebbed hands? In other words, what can simple hands and then pre-wings do that presages and evolves into the flight stroke in bats? Fossils do not yet tell us all the details, but enough is known to create hypothetical transitional forms (Fig. 5).

Inverted bipeds
It should be obvious that pre-bats cannot begin to flap their wings unless their forelimbs are freed from typical support duties. Virtually all living bats are inverted bipeds (the rare exceptions are vampire bats and grounded bats ). Their legs and feet of bats have gone through such radical changes that ordinary quadurpedal locomotion impossible for them now.

An evolutionary starting point: the pen-tailed ‘tree shrew’
Ptilocercus (Fig. 2; actually a pygmy civet) is a small, extant, arboreal, quadruped at home both on tree trunks and narrow branches. It seems unlikely that the transition to bipedalism could have happened upside-down on a tree trunk because the hands would still have been used for support. Rather, the transition had to happen while inverted on a horizontal branch or vine (Fig. 2) with only the hind limbs hanging on and the forelimbs free to flap.

Ptilocercus
is the closet tested living sister to bats and dermopterans, like Cynocephalus. Notably, the pen-tail has no trace of any extradermal flight/gliding membranes anywhere on its body. Thus the gliding membrane of Cyncoephalus and the flying membrane of Pteropus are not homologous.

Inverted Flapping
Earlier I found a video of a full-fledged bat flapping on a horizontal branch, not releasing its feet until attaining a horizontal attitude. That’s the best data I’ve found so far for flapping while inverted before flying. (And I’m not forgetting that this bat had a fully evolved set of wings.) By comparison, smaller hands, like those in Ptilocercus, would have been nearly useless for pushing air around.

When an animal is hanging by its feet, no matter how much it ‘flaps’ its little hands and arms it’s not going to go anywhere. It’s not going to find food and it’s not going to find mates.  I don’t see any evolutionary advantages to this sort of behavior, except to reach another branch lower in the tree. And that’s not a major behavior. It can be done from any posture by any tree dweller.

Unlike quadrupedal mammals,
bats can raise their wrists and hands over their backs as part of their flight stroke. Brachiating primates (anthropoids including humans) can lift their hands over their heads, but not over their backs. Bat shoulder flexibility is due both to their elongated clavicles, that extend above/behind the neck, and to the cranial shifting of the acromion process on the scapula (Fig. 3). That removes the scapular block that restricted dorsal humerus abduction. Only bats have this key trait.

Another question: Which key trait came first? The long clavicle? The dorsally open glenoid? The large webbed hand? At present, we just don’t know. We don’t have the fossils.

Which traits were lost in bats? 
As in birds and pterosaurs, the manus in bats is unable to supinate or pronate because the ulna becomes little more than a splint and the radius no longer axially rotates around it. Thus the bat manus is unable to operate in a normal fashion, palmar side in contact with the substrate, pointing in the direction of quadrupedal locomotion, flexing and extending in PIL sets. Rather in bats, birds and pterosaurs the palms face each other when adducted (like clapping), except at maximum extension (abduction, lateral forelimbs) when the palms face ventrally.

Ontogeny recapitulates phylogeny
We don’t have to rely solely on extant adults and fossils. We can also glean data from extant juvenile and embryo bats, which appear to replay the evolutionary journey of bats. We also have behavioral clues to work with.

Newborns
of Ptilocercus are nest-bound, one, two, or three to a nest. Nestlings receive extremely sparse maternal care as she visits her young every other day for no more than ten minutes at a time. The parents themselves are solitary feeders. By contrast, newborn bats are carried by their mothers everywhere they go, and usually only one at a time. Distinct from Ptilocercus, adult bats are communal.

Bat juveniles
do not fly shortly after birth, but do so only as subadults when their wing fingers reach their adult length. By this evidence we can draw an analogy that bat ancestors did not achieve competent flight until they had adult length fingers. The evidence also shows that less than competent flight was good enough to survive and flourish in this new environment devoid of predators and perhaps filled with prey and close net landing sites, like a tangle of branches and vines. The Paleocene insect fossil record is currently underrepresented, but giant ants and beetles are known. Some of these would have been on Paleocene bat menus.

If you’re going to evolve wings like a bat,
you have to stop using them as hands. Whenever a digit extends or membranes develop, they are going to get damaged and become increasingly awkward with increasing size, unless folded, as pterosaurs and birds do. In adult and juvenile bats the carpus rotates the hand posteriorly for complete wing folding. However, the embryo bat manus (Fig. 5) does not appear to rotate and fold in the same fashion. Even so, in the bat embryo there is little indication of inter-metacarpal muscle. Instead that area looks indistinct from the inter-digital membrane. Note the unguals of manual digits 2-5 in all bats, including embryos, are vestiges and not in use.

Lessons from gliding squirrels, dermopterans and sugar gliders
These living mammal gliders are not related to each other and not related to bats. None develop large hands or a flapping behavior. None of these gliders produce thrust while gliding and therein lies the difference with large-handed bats. Furthermore none of these gliders develop a larger clavicle and scapula, which bats use to anchor large flapping muscles.

Why would a sister to Ptilocercus start to flap?
Elephants flap enlarged ears to cool off. Baby birds flap tiny wings to encourage their parents to feed them. Before they could fly, pre-pterosaurs and pre-birds likely flapped to threaten rivals and seduce mating partners. Bats don’t appear to use their wings except to fly, catch insects and perhaps to wrap themselves for insulation from the cold and rain.

Prey Acquisition > Locomotion 
Given the large gap between Ptilocercus and Eocene bats (Fig. 5), along with the present evidence from embryo/juvenile bats, we can only imagine transitional stages starting with an enlarged hand (HTTaxon 1) and continuing to enlarge that hand while developing extradermal membranes (HTTaxon 2). Here’s how the current data can be used to rebuild the missing portions in the evolutionary stages of bat evolution (Fig. 5).

1. The Ptilocercus state – Ptilocercus is an omnivore that pounces on insects that have landed on trees. Ptilocercus grabs its prey with its hands and kills it with its mouth (Fig. 6). That’s pretty much what bats do, too.
2. Hypothetical Transitional Taxon 1 stage – The five fingers are longer here. That increases the ability to grab prey, like a catcher’s mitt (Fig. 7) does with baseballs. The metacarpals were more loosely joined at their carpometacarpal joints and conversely the fingers were bound by webbed membranes creating more flexible mitts. Perhaps lateral extradermal membranes, like those found in gliding squirrels, dermopterans and opossums, also had their genesis at this stage. Flight, such as it was, would have been restricted to close vines or branches. Frantic flapping would have supplemented each glide.
3. Hypothetical Transitional Taxon 2 stage – Only fingers 3-5 are longer here and they form support structures for more extensive wing trailing membranes. At this stage the hand could no longer be used for traditional quadrupedal locomotion, so bats probably became inverted bipeds at this stage. When forced to, bats rested and walked on the medialventral rim of their folded hands with only their thumbs able to grab surfaces, as they do today. Flight duration continued to expand.
4. Icaronycteris state – The lumbar vertebrae were longer. The tail was shorter. The clavicle, chest and scapula were enlarged at this stage. The ulna was a splint. The hand was full-sized and capable of both folding completely and flying competently. Flight duration had no practical limits.

Behavioral stages
The following hypothetical behavioral stages gradually grade from quadrupedal pygmy civets to aerial bats. As you’ll see, bat wings developed principally for prey gathering, whether that prey was on tree branches or in mid-air.

1. Arboreal prey grabbing with small hands then eating at leisure (Ptilocercus).
2. Arboreal prey gathering with larger hands making large sweeping motions toward the body and mouth (the genesis of the flight stroke, Fig. 1) during capture and transfer to the mouth (HTT1).
3. Branch-to-branch or vine-to-vine leaping/flapping with even larger hands. Loss of the tibial malleolus increasing pedal rotation. (HTT2).
4. Tree-to-tree leaping/flapping with even larger hands that could be folded during inverted hanging. At this stage the whole body starts to act like a catcher’s mitt as flying insects are added to the menu. After capture the tail or wing curls in to transfer the prey to a descending skull to bite and kill the prey while on the wing (Icaronycteris).
5. Open air flapping/flying with wings large enough that juveniles/babies could be carried by mothers. Shorter tail and expanded uropatagium adds to the surface area of the ‘catchers mitt’ as these posterior elements are increasingly used for prey acquisition (Myotis) and the wings less so.
6. Radiation/Evolution into various species, some frugivorous, others with echolocation.

All we have to do now
is find fossils of a Paleocene pygmy civet with large fingers, like those of an embryo bat.

References
Jepsen GL, MacPhee RDE 1966. Early Eocene bat from Wyoming. Science 154 (3754): 1333–1339. doi:10.1126/science.154.3754.1333. PMID 17770307.
Le Gros-Clark WE 1926. On the Anatomy of the Pen-tailed Tree-Shrew (Ptilocercus lowii.) Proceedings of the Zoological Society of London 96: 1179-1309.
DOI – 10.1111/j.1096-3642.1926.tb02241.x
Simmon NB, Seymour KL, Habersetzer J, Gunnell GF 2008. Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451 (7180): 818–21. doi:10.1038/nature06549. PMID 18270539.

wiki/Icaronycteris
wiki/Onychonycteris
wiki/Ptilocercus