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

 

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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.

 

 

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

The Origin and Evolution of Bats Part 2

Earlier we looked at basal bats and their closest outgroups. That entry from several years ago has proven to be a weekly and annual favorite among blog posts here at the pterosaur heresies. Part 3 on this subject was posted here.

Today we’ll do the same with newly arranged graphics (Figs. 1,2) principally matching the non-bat, Ptilocercus, to the basal bats, Onychonycteris and Icaronycteris (Fig. 1). I’m surprised I never did this before because the results are illuminating.

Figure 1. Ptilcercus (above) and Icaronycteris (below), sister taxa in the origin of bats.

Figure 1. Ptilcercus (above) and Icaronycteris (below), sister taxa in the origin of bats. Click to enlarge. Despite the similarities of these two, the differences in dent ion and the size of the manus kept scholars from comparing these two taxa directly with one another. Ptilocercus is also close to the flying lemur, which is why its dentition is more like the flying lemur.

In figure 1 the similarities are striking:

  1. skull, torso, pelvis and tail have similar shapes
  2. ribs are flat in both
  3. radius is longer than the humerus in both.
  4. ulna is reduced distally, to no more than one third the width of the radius (as in bats).
  5. carpus rotates posterolaterally in both
  6. the ability to spread the digits so widely that digits 1 and 5 oppose one another by 180º
  7. first manual digit is somewhat thumb-like, able to grasp objects.
  8. tibia longer than femur in both
  9. ankles are more flexible in both. The astragalus and calcaneum move away from stacked one upon the other to more of a  side-by-side configuration.
  10. Pedal digits 2 – 5 are equal in length and their metatarsals follow suit. The pedal unguals also deepen

Now let’s examine the differences. In the bat:

  1. cervicals are more gracile
  2. clavicle is longer and the scapula is larger (for large pectoral flight muscles)
  3. lumbar region is longer
  4. tail is shorter
  5. entire forelimb is longer, especially the hand
  6. hand is webbed
  7. The tibial malleolus (lateral distal process), which restricts ankle rotation in most mammals is not present in bats
  8. tarsals of bats are smaller, the penultimate phalanges are longer and the unguals are larger. Better to hang inverted.
  9. medial digit of the foot loses its ability to oppose the other pedal digits
  10. Onychonycteris develops a new bone arising from the ankle which helps frame the uropatagium.
  11. some bats use echolocation for prey capture
Figure 2. Selected details of Ptilocercus and Onychnycteris.

Figure 2. Selected details of Ptilocercus and Onychnycteris. The spreading of the metacarpals is a synapomrophy.

Remember
Ptilocercus has different teeth because it is more closely related to Cynocephalus, the flying lemur (Fig. 3), which is also not too distant from bats. Despite the appearance of extradermal membranes in dermopterans, it appears that those were obtained convergently in bats.

Figure 3. Cynocephalus, the flying lemur, shares many traits with Ptilocercus and basal bats.

Figure 3. Cynocephalus, the flying lemur, shares many traits with Ptilocercus and basal bats. Note the distally reduced ulna.

Take another look at the bat family tree (Fig. 4).
Ptilocercus
is not another tree shrew, like Tupaia. Ptilocercus is a miniature civet. Tupaia is in the lineage of rabbits. DNA evidence (Tsagkogeorga et al. 2013) supports this tree topology with bats arising from carnivores, like civets.

Figure 2. Bat evolution and origins from the Carnivora/Viverridae. They are sisters to the Pen-tailed tree shrew and colugos among living taxa. Protictis is an extinct outgroup taxon from the Paleocene.

Figure 4. Bat evolution and origins from the Carnivora/Viverridae. They are sisters to the Pen-tailed tree shrew and colugos among living taxa. Protictis is an extinct outgroup taxon from the Paleocene.

The origin of flight
and flapping in bats continues to be a vexing problem. An earlier hypothesis based on current behavior remains unsatisfying.

Interesting YouTube video
on bat cooling in the tropics here. Yes they flap gently to generate a self-directed breeze, but they also lick themselves for evaporative cooling.

Interesting YouTube video on bat flight here.

More tomorrow.

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.
Tsagkogeorga G, Parker J, Stupka E, Cotton JA, Rossiter SJ 2013. Phylogenomic analyses elucidate the evolutionary relationships of bats (Chiroptera). Current Biology 23 (22): 2262–2267.

wiki/Icaronycteris
wiki/Onychonycteris
wiki/Ptilocercus

Origin of bats 2

Updated Sept 20, 2016, with better data on Protictis and more taxa added to the mammal clade. 

One of the most popular blogposts here,
year after year, has been the post on bat origins back in 2011. Nothing has changed since then except for the fact that I have added a few bats and kin to the large reptile tree (Fig. 1, subset) and Protictis has moved to the Carnivora following better data.

Figure 2. Bat origins cladogram. Here Onychonycteris and Pteropus represent bats.

Figure 2. Bat origins cladogram. Here Onychonycteris and Pteropus represent bats.

And here (Fig. 2), for good measure are Chriacus and Onychonycteris, a bat ancestor candidate and a basal bat respectively, according to the large reptile tree.

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 nests as a sister to the undiscovered bat ancestor. Onychonycteris was 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. Click to enlarge.

 

Phylogenetic miniaturization contributed to bat origins. The teeth became better adapted to insect eating. The larger scapulae and clavicles anchored larger muscles. The ulna became reduced relative to the radius and fused to it. The hands became enlarged. Membranes spanned the forelimbs and hind limbs. This is the only flapper that did not have an obvious bipedal phase.

It is still a mystery what evolutionary events spanned these two taxa. The rest has to be imagined.

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

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

The earliest bats – svp abstracts 2013

From the abstract
Padian and Dial (2003) wrote: “Reconstructing ancestral character states in the evolution of chiropteran flight is challenging because, whereas the earliest bats are clearly capable of flight, their immediate laurasiatherian outgroups provide no useful information about intermediate states between fully volant bats and their terrestrial ancestors. To date, the postcrania of early bats have received less attention than the skull and teeth, and the principal problem addressed has been whether flight preceded echolocation. New preparation of the postcrania of the most basal bat Onychonycteris and comparative character analysis of other basal fossil bats (Icaronycteris, Palaeochiropteryx) reveal a variety of unusual morphological features that shed light on the functional and ecological origin of bats. Newly revealed anatomical features of Onychonycteris and comparative re-examination of other basal bat postcrania demonstrates that the trochanters of the proximal ends of the femur in Onychonycteris were not typically mammalian but subequal, and the head was offset laterally, as in crown-group bats, indicating a relatively “modern” hip flexure and a lateral orientation of the hindlimb. However, details of the tarsus and the claws, both manual and pedal, in these basal bats suggest a different ecological context than would be evident from the basal conditions of living crown-group bats. The functional morphology of the forelimb and hindlimb indicate scansorial habits that imply climbing tree trunks and rock faces. Phylogenetic analysis, integrated with analysis of functional traits, suggests a sequence of simplification and reduction of claws, coupled with increase in wing size, and an eventual shift from generalized scansorial habits to inverted perching on substrates that led to the unusual pedal claw morphology seen in most living bats today.”

Figure 2. Family tree of bats, primates, insectivores and some carnivores, focused to find the ancestors of bats by restricting the inclusion set to arboreal mammals. This tree differs from the more comprehensive O'Leary et al. tree and also shares some similarities.

Figure 1. Family tree of bats, primates, insectivores and some carnivores, focused to find the ancestors of bats by restricting the inclusion set to arboreal mammals. This tree differs from the more comprehensive O’Leary et al. tree and also shares some similarities.

Notes
There’s a DNA vs morphology battle out there with regard to bats and their kin. Volitantia is the morphological clade uniting bats and dermopterans. Here’s how bat expert Eric Sargis reported the battle with documentation.

Sargis 2002 reported, “Based on morphological evidence, one must conclude that the sister taxon of Dermoptera is Chiroptera, not Primates (Szalay, 1977; Novacek, 1982, 1986, 1989, 1990, 1992, 1993, 1994; Novacek and Wyss, 1986; Wible and Covert, 1987; Novacek et al., 1988; Wible and Novacek, 1988; Thewissen and Babcock, 1991, 1992, 1993; Johnson and Kirsch, 1993; Szalay and Lucas, 1993, 1996; Wible, 1993; Simmons and Quinn, 1994; Simmons, 1995; Shoshani and McKenna, 1998; Kriz and Hamrick, 2001; Sargis, 2001b, in prep.; Silcox, 2001a,b, 2002; contra Beard, 1989, 1993a,b; McKenna and Bell, 1997).

Sargis 2002 also reported, “Alternatively, molecular evidence has continually rejected Volitantia (Cronin and Sarich, 1980; Adkins and Honeycutt, 1991, 1993; Honeycutt and Adkins, 1993; Allard et al., 1996; Porter et al., 1996; Liu and Miyamoto, 1999; Waddell et al., 1999; Liu et al., 2001; Murphy et al., 2001a,b), and it is certainly possible that  dermopterans and chiropterans evolved their similarities independently in relation to gliding and flying, respectively. If this is the case, then Volitantia is also an unnatural grouping based on convergent, rather than homologous, characters.”

Sargis 2002 also reported, Molecular evidence, on the other hand, has repeatedly supported a Scandentia-Dermoptera clade (Liu and Miyamoto, 1999; Liu et al., 2001; Madsen et al., 2001; Murphy et al., 2001a,b) with Primates as the sister taxon to this clade (Liu and Miyamoto, 1999; Liu et al., 2001; Murphy et al., 2001a,b).

It keeps getting less traditional, more heretical.
Ptilocercus is not related to other tree shrews (Tupaia) in the bat tree (Fig. 1).

Phylogenetic analysis (the bat tree) nests Chriacus (this taxon as noted by Halliday et al. 2013), and the extant Ptilocercus and the long-legged Cynocephalus as the closest sister groups to bats among those that have limbs. The latter two nest together in molecular studies (Olson et al. 2005) outside of the Scandentia (typical tree shrews). We looked at bat origins earlier here based on morphological, not DNA evidence.

As noted earlier, pterosaurs and birds had bipedal ancestors. If bats did too, even inverted as they configure themselves nowadays, that differentiated them from quadrupedal ptilocercids and dermopterans.

The hypothetical origin of bats likely resembled the taxa here (Fig. 2). I have no answer for why DNA doesn’t match morphology in bats, basal lizards and turtles, among other clades. But if you look up Ptilocercus on ReptileEvolution.com, you’ll be amazed how bat-like it is (and how unlike Tupaia, it is). And Cynocephalus even more so in certain respects.

The evolution of bats beginning with Nandinia.

Figure 2. The evolution of bats beginning with a sister to Nandinia. Click to enlarge.

References
Halliday T, Upchurch P and Goswami A 2013. A phylogenetic analysis of palaeocene mammals. Journal of Vertebrate Paleontology abstracts 2013.
Padian K and Dial KP 2013. New morphological data illuminate hindlimnb function and the ecological context of flight in the earliest bats. Journal of Vertebrate Paleontology abstracts.
Sargis EJ 2002. The Postcranial Morphology of Ptilocercus lowii (Scandentia, Tupaiidae); An Analysis of Primatomorphan and Volitantian Characters. Journal of Mammlian Evolutin 9(12):137-159.

Bat Origins and DNA

Updated September 30, 2016 with the addition of taxa to the LRT and new data on Protictis.

Where DO Bats Nest? The Question Returns.
A renowned (unnamed) professor interested in the origin of bats questioned my morphological nesting of bats with Ptilocercus and Nandinia (among living taxa) and Palaechthon (among fossil taxa). The professor sent me a pdf of Meredith et al. (2011), the most recent DNA tree to lump and split living mammals, as his best hypothesis on bat origins.

Bats and their sisters

Figure 1. Bats and their sisters according to Meredith et al. 2011.

Mammal Diversification
Meredith et al. (2011) sought diversification patterns and times in mammals. They constructed a molecular supermatrix for mammalian families and analyzed these data with likelihood-based methods and relaxed molecular clocks. Their results came in traditionally, with Monotremata, Marsupialia and Placentalia at the base. The latter was divided into Xenartha + Afrotheria and all other placentals, which were divided into Laurasiatheria and Euarchontoglires.

DNA Results for Bats
Lots of bats were tested and they all lumped together in a single clade subdivided into three with fruit bats (Fig. 1 in orange) separating two microbat clades (in blue and green). Bats appeared as the unresolved sisters to Carnivora and Artiodactylia. Basal insectivores (not shown hre) nested as outgroup taxa to this super clade.

That’s an overly general nesting for bats that doesn’t provide much insight. On the other hand, I wasn’t surprised to see bats nesting so close to basal carnivores, like Nandinia and the vivverids, because the morphological results recovered the same relationship. I was surprised to bats nesting close to rhinos and camels.  :-) Pangolins are indeed close to bats, so we agree here (Fig. 2).

Figure 2. Bat origins cladogram. Here Onychonycteris and Pteropus represent bats.

Figure 2. Bat origins cladogram. Here Onychonycteris and Pteropus represent bats.

DNA Results for Flying Lemurs
The base of the Euarchontoglires (Meredith et al. 2011, not shown in Fig. 1) included tree shrews and demopterans. I wasn’t surprised to see rabbits nesting close to Tupaia, the common tree shrew, because the morphological results recovered the same relationship. I also wasn’t surprised to see Ptilocercus, the pen-tailed tree shrew, nesting close to the flying lemurs, because the morphological results recovered the same relationship. Note these taxa didn’t nest with bats in the DNA study, but they did all nest at or near their unresolved common base.

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

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

Morphological Results
The Meredith et al. (2011) results do not match the morphological evidence, which derives both bats and flying lemurs from a sister to Ptilocercus, a Paleocene pro primate and Chriacus, all close to basal carnivorans like NandiniaNandinia is a living carnivore that sometimes drops from trees and has an omniovorous diet. Chriacus was a long-legged tree-dwelling omnivore. Phylogenetic bracketing indicates that post-cranial characters were something like Chriacus and/or PtilocercusPtilocercus is a flying lemur ancestor, but shares with bats several characters including flat ribs, a high floating scapula, wide cervicals, a rotating carpus and metatarsal + phalanx ratio similarities.

The question is…
why don’t the DNA results more closely match the morphological results, and vice versa?

DNA results cannot include fossil taxa. With bats evolving prior to the Eocene (52 mya), fossil taxa are necessary in any study on bat evolution.

The DNA of modern tree shrews and bats, etc. is not the same as the DNA of Paleocene tree shrews and bats, etc.

The Meredith et al. (2011) evidence indicates that DNA results for large clades of mammals  cannot resolve large clades. DNA and amino acid results do not agree with one another in the case of large reptile clades and the same is true in large mammal clades. DNA and amino acids apparently become more useful the more closely taxa are related. The resolution is very high, for instance, in human DNA, which is why it can be used in criminal investigations.

On the Other Hand
In fossil evidence you can point to a long list or suite of homologous morphologies, from tooth cusps to phalanx ratios. DNA results cannot provides these details. Morphology will always trump DNA, especially when bats nest with camels in DNA studies. DNA can only be verified with morphological evidence. DNA results can guide our efforts but the bottom line is morphology. The Meredith et al. (2011) study was unable to provide a specific sister taxon to bats. The morphological study provided Chriacus. When closer sisters are discovered, they will be reported.

Dermopterans and Bats
Flying lemurs nested close to bats and bat babys have short fingers like those of flying lemurs. Problem is: Ptilocercus, which comes between the two, has no extradermal membranes or webbed fingers and its limbs are not elongated. I have no answers for that other than both bats and flying lemurs are about 60 million years old and likely had a common long-limbed ancestor with extradermal membranes in a sister to Ptilocercus. Or bats and flying lemurs both developed extradermal membranes by convergence. Or Ptilocercus lost its ancestral long limbs and membranes.

Can we trust results?
In science we don’t trust anything. Not DNA. Not morphology. Everything is tentative and provisional.

 

References
Meredith RW et al. 2011. Impacts of the Cretaceous Terrestrial Revolution and KPg Extinction on Mammal Diversification. Science 334:521-524.