The origin of flight in bats: what we knew in 1992.

Famous for his whale studies,
JGM (Hans) Thewissen turned his attention to bats as a postdoctoral fellow in 1984. His co-author, SK Babcock, was a graduate student at the time.

Their introduction
includes their intention of reviewing then current controversies despite “extremely sparse” fossil evidence. They mentioned the hundreds of Eocene bat skeletons known from the Messel quarry near Darmstadt, Germany, but note that even late Paleocene bats were “nearly as specialized as their modern relatives.”  Their report preceded by several years the publication of Onychonycteris (Simmons, Seymour, Habersetze and Gunnell 2008), the most primitive bat known at present.

Two kinds of bats were noted, Megachiroptera and Microchiroptera.
“Megabats have a simple shoulder joint and a clawlike nail on thumb and index finger, whereas mi-crobats have a complicated shoulder joint and a claw only on the thumb.” Microbats use echolocation to eat insects with their sharp crested teeth. Megabats generally do not, but a few do. They are herbivores with blunt molars.

Earlier we looked at
the dual origins of turtles,  whales, seals and the four origins of the “pterodactyloid”-grade pterosaurs. Workers have wondered if mega bats and micro bats also had dual origins.  This was the main theme of the Thewissen and Babcock paper, penned before the widespread advent and adoption of computer-based phylogenetic analysis. Instead, everyone looked at a few to many traits and pulled a Larry Martin. Sometimes they were right. Othertimes, they were wrong to slightly wrong. Smith and Madkour 1980 first proposed a dual origin for bats by looking at the penis.

Thewissen and Bacock renege on their headline promise when they report,
“If the problem of bat origins is ever solved, it will be after a careful anal-ysis of all characterso f interesti n the bats and their potential relatives.” Of course this was shortly  before PAUP and MacClade came on the scene the same year.

Thewissen and Babcock report:
“Both microbats and megabats have a propatagial muscle complex, but it is surprisingly different in the two groups.” In mega bats this complex has four proximal origins,

  1. the back of the skull
  2. the side of the face
  3. the ventral side of the neck and
  4. the midline of the chest

compared to only two origins in micro bats (1 and 4). There is also variation within micro bats and within mega bats. As readers know, there is no way to understand this unless outgroups have one or the other pattern and they don’t (at present). Thewissen and Babcock report, “gliding flight has evolved six times in mammals.” But gliders don’t make good flyers. To fly one needs thrust provided by flapping. How and why bats started flapping has really been the key underlying, unanswered question, which we looked at earlier here and here.

Back in 1910
WK Gregory concluded after careful study that bats, flying lemurs, tree shrews, elephant shrews and primates were closely related and called that group (clade) Archonta. According to the large reptile tree (LRT, 1043 taxa) many of these taxa are indeed related. Elephant shrews are not, which Thewissen and Babcock later note. Elephant shrews are also the only ones from that list that are not arboreal climbers. Thewissen and Babcock add the clade Plesiadapiformes, which were thought to be rodent-like primates, but turn out to be primate-like rodents nesting close to multituberculates in the LRT.

Figure 1. Bat cladogram. Here pangolins are the nearest living relatives of bats.

Figure 1. Bat cladogram. Here pangolins are the nearest living relatives of bats.

Flying lemurs,
like Cynocephalus, also have a propatagium that originates from the side of the face and midline of the neck, but the nerves within them terminate in different places in bats. The LRT recovers flying lemurs close relatives to bats, but pangolins, like Manis, are closer.

Thewissen and Babcock conclude: 
“We believe that the evidence from the propatagial muscle complex of bats supports the idea that all bats share a single ancestor with wings. This idea is consistent with bats going through a flying lemur-like stage before acquiring active flight.”

Unfortunately
the LRT recovers a topology in which the last common ancestor of flying lemurs and bats was likely arboreal, but not a leaping glider. That means membranes developed in parallel (close convergence). Remember, gliders don’t become flappers. And flappers usually develop flapping for reasons other than flight, then co-opt flapping traits for flight.

The ancestors of bats and pangolins
have had a long time to diverge. Likely that was in the Late Jurassic because we have the pangolin ancestor, Zhangheotherium, appearing in the Early Cretaceous. That puts the last common ancestor of flying lemurs, pangolins and bats, Ptilocercus, back in the Middle Jurassic, several tens of millions of years after the likely first appearances of therian mammals, like the living and very late surviving Didelphis and Monodelphis sometime in the Early Jurassic. Earlier we looked at the origin of bats here, here and here.

Figure 2. Select basal cynodonts and mammals set chronologically. The divergence times for placentals (Eutheria), marsupials (Metatheria) and monotremes (Mammalia) are estimated here.

Figure 2. Select basal cynodonts and mammals set chronologically. The divergence times for placentals (Eutheria), marsupials (Metatheria) and monotremes (Mammalia) are estimated here.

References
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.
Smith, J. D., and G. Madkour. 1980. Penial morphology and the question of chiropteran phylogeny. Pages 347-365 in D. E. Wilson and A. L. Gardner, eds. Proceedings of the 5th International Bat ResearchC onference. Texas Tech Press, Lubbock.
Thewissen JGM and Babcock SK 1992. The origin of flight in bats. BioScience 42(5):340–345.

wiki/Onychonycteris

 

Better data on Protictis shifts it from bats to carnivores

Updated January 06, 2016 based on additional taxa.

This is what happens
when you get data more directly. In this case data that used to come from a freehand drawing (Fig. 1) now comes from a photo of Protictis (Cope 1883, Mac Intyre 1966; middle Paleocene; Fig. 1). As everyone knows, in Science, you have to be willing to let go of any pet hypotheses of relationships whenever better data recover different results. And this is how you do it: You just do it!

Figure 1. Protictis skull based not on a free hand drawing, but on this published photo.

Figure 1. Protictis skull based not on a free hand drawing, but on this published photo from Mac Intyre 1966. Note all difference with the original freehand drawing, also from Mac Intyre 1966. Preserved elements about 5 cm in length.

More than five years ago,
before ReptileEvolution.com was first created with about 260 taxa in the large reptile tree (now 915 taxa), Protictis was not included in that data matrix. Rather it nested in a separate ‘bat’ cladogram between Chriacus and bats based on data gleaned from the line art reconstruction in Mac Intyre 1966  Now Protictis joins the LRT with data based on a published photo (Fig. 1) in Mac Intyre 1966. Now it nests with Vulpavus, Deltatherium and the carnivore specimen of Ectocion. all within the Carnivora. That makes sense based on several traits, including the very large canine teeth.

That early Palaeocene date
along with the rather derived node occupied by Protictis anticipate (currently without much evidence) a wider radiation of the Carnivora during the Jurassic and Cretaceous than prior workers surmised. An early member of this clade, Vincelestes, is found in Early Cretaceous strata, yet even at that early date, already shows distinctly derived traits. Phylogenetic and chronological bracketing predict that mongoose- and civet-like carnivore taxa will be found in Jurassic and Cretaceous strata.

I’ll have to go back and update
any figures that have not yet been updated. Here (Fig. 2) is the latest on bat origins (now sans Protictis). And there’s more here. It’s the same topology, only without Protictis now.

Palaechthon has been added today
but it nests, as it did before, with the dermopteran, Cynocephalus.

Figure 2. Known bat ancestors to scale. Click to enlarge.

Figure 2. Known bat ancestors to scale. Click to enlarge. Protictis is no longer among them. It is likely that bat ancestors never got as large as Chriacus, but it is the only representative of that morphology, between Ptilocercus and bats.

And we can still use Ptilocercus as a pretty good model
for bat origins. It nests close to their ancestry without showing signs of great deviation.

Figure 4. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you're going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

Figure 3. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you’re going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

 

References
Cope ED 1882. Synopsis of the Vertebrata of the Puerco epoch. Proceedings of the American Philosophical Society 20:461-471.
Mac Intyre GT 1966. The Miacidae (Mammalia, Carnivora) Part 1. The systematics of Ictidopappus and Protictis. Bulletin of the American Museum of Natural History 131(2):115-210.

The origin and evolution of bats, part 4, an inverted thought experiment

There are no fossils
that currently document the origin of bats from non-volant carnivores or omnivores. Birds have a long fossil history. So do pterosaurs. For bats we have to conduct thought experiments in order to get from points we know: 1) a skilled arboreal omnivore like Ptilocercus, to 2) an Eocene fossil bat, like Icaronycteris (Fig. 1). It won’t help to have a Paleocene tooth, or skull. Those don’t change much in bat origins. We need to see, or visualize, the post-cranial body. Earlier forays into bat origins can be seen here, here and here.

Figure 1. GIF animation thought experiment on the origin and evolution of bats from a Ptilocercus-like omnivore.

Figure 1. GIF animation thought experiment on the origin and evolution of bats from an inverted Ptilocercus-like omnivore. Click to enlarge. Perhaps long fingers originally pulled maggots out of fruit and excellent hearing helped probate find where to dig.

We start with what we know

  1. All or most bats hang inverted
  2. The basal phylogenetic split is between Megachiroptera (fruit eaters) and Microchiroptera (insect eaters)
  3. Bat embryos probably recapitulate the development of those unknown phylogenetic predecessors, And they have big webbed hands early on.
  4. Bats don’t fly until their wings are nearly full size.
  5. What separates Ptilocercus from Icaronycteris is chiefly the size of the hands.
  6. There is no evidence that bats find their wings or wing size sexually attractive
  7. Caves are derived roosting spots. You have to fly in those to get a spot.
  8. Likewise, catching insects on the wing and echolocation follows the advent of flying, but listening to maggots munching fruit might have been a precursor skill.

The big question has always been
how do you get a flight stroke out of quadruped? Pterosaur and bird ancestors were both bipeds with strong hind limbs and they evolved wings as 1) gaudy secondary sexual traits; and 2) to aid in locomotion, especially up steep inclines (Heers et al. 2016 and references therein). The only way that bats were bipeds was inverted with weak hind limbs, which is a whole different story, or, in this case, a whole different thought experiment.

Figure 2. Pteropus, a fruit bat.

Figure 2. Pteropus, a fruit bat, has relatively shored clavicles and larger scapulae extending over most of the rib cage. The extremely long toes are derived. Parallel interphalangeal joints present on bat wings show the phalanges flex in sets.

Hypothetical stages in bat development

  1. Start with an agile arboreal omnivore like Ptilocercus, derived from long-legged arboreal carnivores in the Cretaceous/Paleocene, like Chriacus.
  2. Hanging fruit and the maggots therein can be attacked by likewise hanging on the supporting branch.
  3. The tiny hands of Ptilocercus could hold the fruit more steadily if the f fingers were longer. Maybe digging out maggots was aided by longer, thinner fingers.
  4. Webbing on even longer fingers would help trap juices, pieces, maggots from dropping out, and (see #6).
  5. At this stage the inverted biped no longer uses those hyper-elongate fingers for climging, so they are capable of being folded, not from the metatarsophalangeal joint, but at the wrist.
  6. In tropical forests bats use their wings as fans to cool themselves off (see video here), often after salivating on themselves for evaporative cooling. This is one of two pre-flight-stroke actions I have found.
  7. To rise from an inverted position on a branch, bats will flap vigorously (Fig. 3), which is the other pre-flight-stroke action.
  8. Mother bats wrap developing infants in their folded wings, but that doesn’t get them into the air.
  9. At a certain point, the pro-bat has wings that are capable of fanning the air, but incapable of flying. This is when the first branch-to-branch and tree-to-tree flapping leaps took place. If the pro-bat falls to the ground, it dies. Only successful arboreal flapping ‘acro-bats’ survive and improvements increase those odds.
Figure 1. Is this the origin of bat flapping. From an inverted position, this bat rises to horizontal by flapping, still clinging to its perch until release and flight. Click to open video.

Figure 3. Is this the origin of bat flapping. From an inverted position, this bat rises to horizontal by flapping, still clinging to its perch until release and flight. Click to open video.

In summary,
hanging pro-bats first developed long fingers to hold hanging fruit and perhaps remove maggots. Fanning for cooling could only develop with large webbed hands. Vigorous flapping from an inverted configuration is one solution to elevating the head and body. Letting go with the feet during this activity is the first awkward and potentially lethal stage to ultimately perfecting the flight stroke over many generations. The origin of flapping in bats is only a thought experiment at present with no other evidence currently available.

References
Heers AM, Baier DB, Jackson BE & Dial  KP 2016. Flapping before Flight: High Resolution, Three-Dimensional Skeletal Kinematics of Wings and Legs during Avian Development. PLoS ONE 11(4): e0153446. doi:10.1371/journal.pone.0153446
http: // journals.plos.org/plosone/article?id=10.1371/journal.pone.0153446

New fossil bats video from the Royal Tyrrell Museum: Dr. Gregg Gunnell

The origin of bats
has been THE hottest topic here at the PterosaurHeresies.Wordpress.com blogsite. See earlier posts here, here and here.

“Fossils of the Night – The History of Bats Through Time” is a new YouTube video (53 minutes) brought to you by Dr. Gregg Gunnell from Duke University, speaking in the Royal Tyrrell Museum series on prehistoric topics.

Dr. Gunnell reports:

  1. only one extinct genus of fruit bat/flying fox
  2. 40+ extinct microbats (all echo-locators)
  3. Bats not close to primates, but with carnivores, hooved mammals, etc. (pretty broad!)
  4. Origin to 65 mya according to molecular clock
  5. Appear at 52 mya. We lack bat fossils from the Paleocene
  6. 11 extinct families of bats
  7. Icaraonycteris and Onychonycteris are two of the oldest known fossil bats. (Eocene, 52 mya) complete
  8. Messel bats (48 mya) more or less complete.
  9. More recent bats are bits and pieces, mostly dental taxa
  10. None of these are directly related to living families
  11. By the Pliocene nearly all modern taxa are known from fossils.
  12. Brachial index (forelimb/hindlimb ratio) midway between non-volant and flying mammals.
  13. CT scans of the teeth were made. All the inner halves of the teeth are crushed into small pieces.
  14. Certain lacewings, both extinct and extant, have a auditory organ on the wings that enables them to detect bat sonar. They stop flying when bats are detected.
  15. Bats have a low metabolism for their size. They live for up to 40 years.
  16. Smaller size increases wingbeat and sonar frequencies
  17. ‘Phyletic nanism’ describes body size decrease, island dwarfism. Onychonycteris was 38-40g. Microbats run about 14g.
  18. Gunnell reports on Yi qi, accepting the patagium/extra wrist bone hypothesis, which was falsified here.
  19. The origin of bats — Dr. Gunnell reports we don’t know what came before Onychonycteris.
  20. Nice morph video (5 seconds) of an inverted mammal on a tree trunk turning into a bat at the very end of the presentation.

This origin agrees with the large reptile tree,
which pulls both bats and primates out of carnivores. Here (Fig. 1) the extant Ptilocercus is employed as a model bat ancestor morphotype.

Figure 4. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you're going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

Figure 1. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you’re going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

 

 

A new hypothesis on bat ancestry: seems odd…

Halliday, Upchurch and Goswami (2015)
report they have resolved the relationships of Paleocene placental mammals. That includes bats, of course (subset of their cladogram in Fig. 1).

From their abstract “the affinities of most Paleocene mammals have remained unresolved, despite significant advances in understanding the relationships of the extant orders, hindering efforts to reconstruct robustly the origin and early evolution of placental  mammals. Here we present the largest cladistic analysis of Paleocene placentals to date, from a data matrix including 177 taxa (130 of which are Palaeogene) and 680 morphological characters.”

The ancestry of bats
has been a traditional problem in paleontology. Pterosaur Heresies resolved that to a certain extent here and here. Halliday et al. put forth a new and odd sister taxon, Apatemys (Fig. 2), a small chisel-toothed mammal. Unfortunately the only time Apatemys is mentioned in the text is in the cladogram figure.

Figure 1. A subset of the Halliday et al. 2015 tree attempting to resolve relationships of placental mammals. Here the proximal outgroup for three bats is Apatemys (figure 2).

Figure 1. A subset of the Halliday et al. 2015 tree attempting to resolve relationships of placental mammals. Here the proximal outgroup for three bats is Apatemys (figure 2).

As readers may recall, 
the large reptile tree nested bats with the extinct arboreal carnivores, Vulpavus and Chriacus (Fig. 3) and the small extant mammal Ptilocercus, which we looked at here. In the Halliday et al. tree, Vulpavus nests on a nearby busy branch. Chriacus nests much farther away. Ptilocercus nests as a very basal mammal with Plesiadapis, Notharctus and other primates, far from Tupaia, which nests with Cynocephalus (just the opposite of what the large reptile tree recovered, which aligned Tupaia with rabbits and Ptilocercus with flying lemurs like Cynocephalus.

Figure 2. Apatemys nests as a proximal sister to bats in the Halliday et al. tree. But it shares very few traits with bats. Note the very odd dentition.

Figure 2. Apatemys nests as a proximal sister to bats in the Halliday et al. tree. But it shares very few traits with bats. Note the very odd dentition that no bat shares. This specimen nested with Tupaia, Plesiadapis and other insectivores.

A more generalized and bat-like dentition
is found in Chriacus  (Fig. 3). Unfortunately the fossils are few in the ancestry of bats. We have to work with what we have.

Figure 1. Hypothetical bat ancestors arising from a sister to Chriacus, which may be a large late survivor of a smaller common ancestor.

Figure 1. Hypothetical bat ancestors arising from a sister to Chriacus, which may be a large late survivor of a smaller common ancestor.

The next most proximal outgroups to bats
in the Halliday et al. cladogram include the digging taeniodont Onychodectes and the basal pangolin Escavadodon (Fig. 1, 4). Again, these are all much more derived than a sister to bats needs to be. They are not at all ‘bat-like’. Not sure why the Halliday team arrived at such an odd nesting. It doesn’t appear to make sense. I don’t see any gradual accumulation of derived traits leading up to bats here.

Figure 4. Onychodectes and Escavadodon nest as penultimate outgroups to bats in the Halliday et al. tree, but they really should have nested much further away.

Figure 4. Onychodectes and Escavadodon nest as penultimate outgroups to bats in the Halliday et al. tree, but they really should have nested much further away. Do you agree?

On the other hand
Ptiilocercus (Fig. 5) is still the best example of what a bat ancestor must have looked like, as we examined previously here, here and here.

Figure 4. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you're going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

Figure 5. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you’re going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

Ptilocercus is the right size,
the right niche, and it has lots of bat-like traits, like that rotating wrist, flat ribs and that high floating scapula.

References
Halliday TJD, Upchurch P and Goswami A 2015. Resolving the relationships of Palaeocene placental mammals. Biological Reviews first published Dec 21, 2015.

 

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 various 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 succeed at 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.

Figure 1. Bat flight stroke in anterior view. This is a different stroke than birds or pterosaurs used, depending more on elbow and finger  flexure and extension.

Figure 1. Bat flight stroke in anterior view. Note how the wing tips gather toward the torso during part of the flight stroke.  Click to view YouTube video. Note the elbows don’t move a great deal here, but the wrist rises above the back, unlike other mammals.

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) gathering prey like a catcher’s mitt.

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 small pre-wings do that presages and evolves into the flight stroke we see in bats with large wings? 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). The legs and feet of bats have gone through such radical changes that ordinary quadrupedal locomotion is 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.

Figure 3. The pen-tailed tree shrew, Ptilocercus, the closest living non-flying relative of bats. Note the pose, perpendicular to the narrow branch. It arrived there by leaping from one branch to another, rather than walking along the length of the branch. When pen tails 

Figure 2. The pen-tailed tree shrew, Ptilocercus, the closest living non-flying relative of bats. Note the pose, perpendicular to the narrow branch. It arrived there by leaping from one branch to another, rather than walking along the length of the branch.

Figure 3. Bat and human scapula compared. Red arrows point to acromion process, reduced and moved away from the shoulder joint in bats to enable greater freedom of motion.

Figure 3. Bat and human scapula compared. Red arrows point to acromion process, reduced and moved away from the shoulder joint in bats to enable greater freedom of motion.

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, but developed independently.

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 attract mates. I don’t see any evolutionary advantages to this sort of behavior.

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 only 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.

Figure 3. Fruit bat (Pteropus) skeleton with hypothetical muscles added).

Figure 4. Fruit bat (Pteropus) skeleton with hypothetical muscles added).

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 as they grow up. Their wings are much smaller than in adult bats. We also have behavioral clues to work with.

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

Bat juveniles
do not fly shortly after birth, but do so only as subadults when their wing fingers reach 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 that Paleocene environment devoid of predators and likely filled with prey and nearby landing sites. Picture a tangle of branches and vines with pre-bats leaping and flapping between them.

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.

Figure 4. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you're going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

Figure 5. Ptilocercus, Icaronycteris and two hypothetical transitional taxa based on the ontogenetically immature wing of the embryo Myotis. If you’re going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

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).

Figure 5. Ptilocercus in vivo, holding prey with its small hands while eating it.

Figure 6. Ptilocercus in vivo, holding prey with its small hands while eating it.

  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 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. 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 in a rudimentary fashion.
  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 now transforming into flying organs. Loss of the tibial malleolus increases 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 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.
Figure 7. Everything evolves, even catcher's mitts. By analogy, bat's wings evolved to become better catcher's mitts.

Figure 7. Everything evolves, even catcher’s mitts. By analogy, bat’s wings evolved to become better catcher’s mitts. Click to enlarge.

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

Is this the origin of bat flapping?

Updated Sept 30, 2016 with the shifting of Protictis to the Carnivora. 

Here on this YouTube video
is a bat hanging upside-down on a branch (Fig. 1). And then it takes off and flies. At first it doesn’t go anywhere, but it is flying/hovering after the feet finally let go of the branch.

Note, like roterosaurs and birds,
the bat is also bipedal — only upside-down, so balancing on hind limbs is not an issue for bats. Hanging upside down is nearly universal in bats.

Figure 1. Is this the origin of bat flapping. From an inverted position, this bat rises to horizontal by flapping, still clinging to its perch until release and flight. Click to open video.

Figure 1. Is this the origin of bat flapping. From an inverted position, this bat rises to horizontal by flapping, still clinging to its perch until release and flight. Click to open video.

With bipedal birds and pterosaurs,
wings appeared to develop first as decorative ornaments and flapping appears to have developed as a secondary sexual behavior to enhance feathers, plumes, hairs, and membranes already in place.

Bats were never glitzy.
They were always dull and brown. They never developed elaborate pre-sex mating rituals. They were never visual creatures. So elaborate frills and colors never appeared on them.

Since bats hang bipedally inverted,
their forelimbs and especially their hands were free to develop into something else. In this case foldable wings. But to get there, everyone knows, there had to be transitional phases in bat evolution, each phase fully functioning and conferring a competitive or survival advantage. Those transitional phases have not been discovered yet in the fossil record, nor have they been visualized. One problem has been a lack of phylogenetic bracketing, which only reptileevolution.com has provided (Fig. 2, as far as I know). Even so this is a fairly broad bracket.

Figure 2. Chriacus and Onychonycteris nest as a sister to the undiscovered bat ancestor and a basal bat. Miniaturization was part of the transition. So was enlargement of the manus. It is still a mystery why the transitional form decided to start flapping.

Figure 2. Chriacus and Onychonycteris nest as a sister to the undiscovered bat ancestor and a basal bat. Miniaturization was part of the transition. So was enlargement of the manus. It is still a mystery why the transitional form decided to start flapping.

Taxa in our phylogenetic bracket:
At present we have Chriacus without wings and Onychonycteris with wings. 

Figure 4. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you're going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

Figure 4. Ptilocercus, Icaronycteris and a hypothetical transitional taxon based on the ontogenetically immature wing of the embryo Myotis. If you’re going to evolve wings it looks like you have to stop using them as hands early on. Note in the bat embryo there is little indication of inter-metacarpal muscle. That area looks identical to the web.

Chriacus did not flap. Onychonycteris did.
Both were arboreal, long-limbed mammals. The big question everyone has been wondering is the how and why for transitional taxon flapping.

In the above video
we can see the inverted bat rising to a horizontal configuration while flapping and maintaining its perch with its hind limbs. This same action could be done with smaller wings in incremental steps, with advancements originating with little to no membrane and improving to a full-fledged membrane and extended fingers.

Note,
in pre bats this would not be considered flying. Instead it might be considered rowing through the air. And, except for grounded bats, there is little to no contribution from the hind limbs in becoming airborne. Instead, they simply let go. This is in direct contrast to colugos, Ptilocercus, primates, and arboreal pre-rabbits, all of which had leaping hind limbs. 

The next question is,
why would an inverted bat want to rise to a horizontal configuration when it has no intention of flying?

To get to the other branch
when a pre-bat detected an insect on another branch. (Before it could attack flying insects, a prebat had to attack crawling insects, some of which were resting after a flight or were just crawling out of a pupae or hive.)

The above video was taken in a lab environment
with a single branch and a single bat. In the natural world of the Paleocene there would have been more branches available (perhaps a tangle of vines and branches). Rising to the horizontal by vigorous flapping would have put other branches within reach. Evidently, once bats had traded grasping hands for flapping hands with grasping thumbs, there was no turning back. A horizontal branch works better than a tree trunk in providing clearance for flapping arms/wings.

Bats are not like slow-moving colugos.
When not hibernating or resting, bats are active little engines of flight. We can imagine their unknown ancestors were also active little predators, with an unusual method for getting around. From vines and branches to open air flying, they took risks, experienced failure as they parachuted into the leaf litter, then climbed another tree to start all over again. Over time some bats found they could reach further branches by flapping faster, with larger strokes with longer fingers provided with broader membranes.

Bat flight is different than bird and pterosaur flight.
According to Tian et al. 2006, “The kinematic data reveals that, at the relatively slow flight speeds considered, that the wing motion is quite complex, including a sharp retraction of the wing during the upstroke and a broad sweep of the fully extended wing during the downstroke. In some respects it is almost like the animal is “rowing” rather than flying!”

In other words,
bats don’t rely so much on