Anderson and Ruxton 2020: the origin of bat flight

Intentionally humorous warning:
Googling “Anderson Ruxton  bats” will likely turn up Andersonbat.com, maker of baseball bats, not relevant to today’s discussion.

Anderson and Ruxton 2020 start their ‘origin of bats’ hypothesis
by describing the origin of flight membranes (as far as is known to them) in insects, pterosaurs and birds, before proceeding to bats. About pterosaurs they write, “This membrane is believed to have been used for display purposes prior to being recruited as flight apparatus, meaning that the wings of pterosaurs would have originated at the distal end of the limb and developed proximally later (Peters 2001).” 

Finally a paper citing Peters 2001! It may be the only paper to consider how pterosaur wings came to be with real taxa. (Also see below for criticism of this citation). The authors note that birds also used their pre-volant wings for display.

Then the authors move on to bats.
When discussing phylogeny, the bedrock of any vertebrate study, they write, “the order Chiroptera has now confidently been arranged as monophyletic and placed within the clade Laurasiatheria (Madsen et al. 2001) along with the order Eulipotyphla (hedgehogs – Erinaceidae, shrews – Soricidae, moles – Talpidae, etc.).” 

Unfortunately, this is wrong. They are citing authorities relying on invalid genetics, rather than finding out for themselves using traits. Bats are not related to ground-dwelling hedgehogs, shrews and moles according to the large reptile tree (LRT, 1734+ taxa). Rather, based on fossils and traits bats arise from arboreal tree shrews, including sisters to extant Ptilocercus (Figs. 2, 3) and extinct Chriacus (Fig. 2).

The authors venture only part of their hypothesis with this statement: 
“Given the apparently idiosyncratic combination of laryngeal echolocation and powered flight present only within the Chiroptera, understanding the evolution of powered flight in the group is inherently linked to understanding the evolution of laryngeal echolocation.”

And…that’s when they go down the rabbit hole. Phylogenetic analysis of traits, not genes, not teeth, not the larynx, provides ALL the clues to the evolution of bats. ‘The Origin of Bats‘ is a topic that has proven overwhelming popular here at PterosaurHeresies. Several hypotheses have been put forth. The latest is here, with links therein to earlier posts.

Again, reading from outdated textbooks,
the authors note, “Both birds and pterosaurs are members of the Sauropsida, the amniote clade that diverged from the Synapsida approximately 310 mya (Kemp 2005), leaving the question: why is powered flight more common in the Sauropsida than in the Synapsida?”

When you add taxa, bats and birds (clade: Archosauromorpha) have a last common ancestor, Vaughnictis, more recent than the last common ancestor of Vaughnictis and pterosaurs (clade: Lepidosauromorpha). That basal reptile split (340 mya) was published online in 2011.

Again, reading from outdated textbooks,
“The Archosauria includes the birds and the pterosaurs, both of which possessed this unidirectional airflow respiratory system (Claessens et al. 2009).”

The authors cite mistake after mistake
without critically reviewing or testing it, “Now, with the recent publication of the discovery of the winged theropod, Ambopteryx longibrachium (Wang et al. 2019), the stage is set for a reexamination of the story of the evolution of flight in bats.” We looked at the wings of Ambopteryx earlier here.

An excellent review
of bat anatomy appears in the Anderson and Ruxton paper with many citations.

When Anderson and Ruxton begin to explain their ‘novel’ hypothesis
they start with a hopeful, but invalid statement, “It is likely that bats evolved true flight from an ancestral gliding state (the aerodynamics of this have been subject to detailed theoretical modelling; Norberg 1985, Hedenstrom & Johansson 2015 and references therein).”

Strangely, the authors never address the inverted biped configuration common to all bats. Nor do they address the dual role of the membranes as juvenile nurseries. Nor do they address the practice of capturing prey in the scoop of the tail, close to the cloaca, rather than the wings. Nor do they discuss the elongation of the clavicles as elongate, locked down coracoid substitutes. Nor do they examine bat embryos. Nor do they address the phylogeny of bat outgroups. You don’t have to be a bat expert to figure this out. Simply add taxa until ‘stem’ bats appear in the cladogram.

The authors note,
“the question of exactly how and why a flapping motion originated from gliding remains unexplained.”  

Flapping never arises from gliding. This sort of myth perpetuation is what happens when young paleontologists have to follow what the textbooks and professors say, instead of thinking and testing all ideas.

So, here’s what Anderson and Ruxton propose:
“The echolocation-first hypothesis proposes that nocturnal pre-bats used a reach-hunting technique to capture flying insect prey. This technique involves reaching out with the forelimbs from a stationary perch and is likely to have involved a complex sensory system to calculate and predict prey movements.”

Pretty ambitious and doing so without resorting to an anglerfish-like illuminated lure to entice insects within range. (Hyperbolic satire there). What Anderson and Ruxton propose is Lamarckism at its worst.

More from Anderson and Ruxton:
“Over time, the echolocation would have become more sophisticated and the forelimbs would extend further and include an interdigital membrane to improve prey capture while the pre-bat remained perched, by creating a larger ‘net’. Gliding and then flight would have developed later, as the pre-bats leapt from their perch to reach insects further away, and echolocation would have been secondarily lost in pteropodids (Speakman 2001).” The authors also cite, Fenton et al. (1995).

This presumes the reward of capturing each insect was worth the price of falling from their perch and climbing up again. Failure to capture each insect every time would have resulted in no reward. A discussion of the leaf litter cushion below each perch would have been appropriate here.

To their credit, the authors note,
“the morphology required to allow gliding is completely different from that of the wings of birds during development and in terms of aerodynamics.”

True.

Flashing forward to the big  Anderson and Ruxton reveal:
“Introducing the interdigital webbing hypothesis.” Then, “it is possible and perhaps likely that these three groups [of bats, see Fig. 1] developed their respective flight and echolocation abilities independently from one another.”

According to Anderson and Ruxton,
the last common ancestor of all bats would have been:

1. nocturnal and using ultrasonic calls for communication
2. highly auditory
3. arboreal with elongated digits and interdigital webbing. On this last point, the authors note, “Interdigital webbing (syndactyly) is one of the most common limb malformations in humans (Malik 2012), and the retention of interdigital webbing is generally not detrimental to the animal.”

According to Anderson and Ruxton,
diverging clades developed like this (see Fig. 1):

1. The rhinolophoid ancestors developed further specialised gliding apparatus proximally and then developed powered flight as part of improved perchhunting.
2. In non-rhinolophoid microchiropterans, powered flight and echolocation developed in tandem.
3. In Pteropodidae (flying foxes) flight developed in tandem with visual acuity.

To their credit, the authors note,
“This interdigital webbing morphology would have been advantageous to pre-bats…   would allow the animal to detect fine-scale information about its substrate, allowing better grip in darkness and perhaps even allowing the animal to detect vibrations produced by the movement of predators or prey along the substrate.” 

This follows the hypothesis generated earlier here (Figs. 2, 3), but does not specify a leaf litter substrate filled with insects and other animals making sounds as they move through it.

Finally the authors cite members of the Dermoptera,
the colugos. “Interdigital webbing makes so much sense in arboreal animals that the Dermoptera exhibit interdigital webbing and, as a result, their particular mode of gliding is known as ‘mitten gliding’, though the majority of lift is provided by a forelimb-to-hindlimb patagium. It is possible that this was the ancestral mode of gliding in chiropterans, and it does not necessarily need to be the case that the interdigital webbing developed prior to the rest of the patagium.”

Unfortunately the authors cite ‘authority’, rather than testing for themselves, when they mistakenly note colugos are genetically distantly related to bats.

Figure 1. Diagram from Anderson and Ruxton 2020 offering their origin of bats hypothesis. This represents the latest (2020) information in the academic literature on the origin of bats. The brown creature is imaginary.

Figure 2. Known bat ancestors and relatives to scale according to the LRT. Click to enlarge.

Figure 3. Starting with Ptilocercus here are several hypothetical transitional taxa leading to Icaronycteris, a basal bat. Note only digits 3–5 contribute to the winging the Myotis embryo. Note also the separation of the finger membranes from the torso membranes.

Anderson and Ruxton conclude,
“Drawing on comparisons from the vertebrates, and in the light of the recently published description of the membrane-winged dinosaur Ambopteryx longibrachium, this interdigital webbing hypothesis provides a biologically satisfying narrative for the evolution of flight in bats, from arboreal mammals to the fastest-flying vertebrates that we know of.”

I’ll conclude by reiterating: The authors never address the inverted biped configuration common to all bats. Nor do they address the dual role of the membranes as juvenile nurseries. Nor do they address the practice of capturing prey in the scoop of the tail, close to the cloaca, rather than the wings. Nor do they discuss the elongation of the clavicles as elongate, locked-down coracoid substitutes. Nor do they examine bat embryos. Nor do they address the phylogeny of bat outgroups. Ptilocercus (Figs. 2, 3) and Chriacus (Fig. 2) are omitted from the text.

Regarding the rare citation of Peters 2001, 
members of the Dinosaur Mailing List had this to say in the past few days:

Thomas Yazbeck: Anderson & Ruxton cite Peters (2001) and seem to accept his very controversial pterosaur – prolacertiform connection at face value. Did they do a deep enough dig into the archosaur literature?

Tyler Greenfield: Anderson stated on Twitter that she wasn’t aware of the problems with Peters’ work when she wrote the paper. This is understandable as she’s not an archosaur researcher.

Mickey Mortimer: In all fairness, that was before Peters became a crackpot/troll, and the lack of any modern engagement with Longisquama (besides the parafeathers), Cosesaurus or Sharovipteryx is a genuine problem he continues to be correct about. I still think such a relationship is plausible.

Note that
Yazbeck cites authorities based on taxon exclusion, rather than his own competitive testing that replicates the taxon list in the Peters 2000, 2001 experiments. Greenfield is closing a wound on Anderson she didn’t know she had. Mortimer has reverted to middle-school name-calling, then turns around and semi-supports the original hypothesis that started this blog. All the above problems can be resolved by simply adding taxa.

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References
Anderson SC and Ruxton DD 2020. The evolution of flight in bats: a novel hypothesis. Mammal Review 1–14. Published by Mammal Society and John Wiley & Sons Ltd.
Peters D 2000b. A Redescription of Four Prolacertiform Genera and Implications for Pterosaur Phylogenesis. Rivista Italiana di Paleontologia e Stratigrafia 106 (3): 293–336.
Peters D 2001(2). A New Model for the Evolution of the Pterosaur Wing – with a twist. – Historical Biology 15: 277–301.

Restoring the skull of the basal bat, Onychonycteris

Short one today,
more ‘show’ than ‘tell’ as one picture and a caption pretty much tell the tale.

Figure 1. Onychonycteris is known from an articulated but crushed bottom half of the skull. Uncrushing it and giving it a suitable top half (Myzopoda) provides a restoration with some possibility of resemblance to theo original. Images from Simmons et al. 2010. The skull could have been less crushed than imagined here, so may have been proportionately shorter. The hole in the braincase of Myzopoda (above) may be a surgical opening to remove brain tissue. If natural, I do not know what it is.

And a cladogram
for phylogenetic context (Fig. 2).

Figure 2. Subset of the LRT focusing on the resurrected clade Volitantia, including dermopterans, pangolins, bats and their extinct kin.

Onychonycteris finneyi (Simmons, Seymour, Habersetze and Gunnell 2008) Eocene (~52mya), ~27 cm in length, is the most primitive known bat. It retained unguals (claws) on all five digits, a primitive trait not shared with other bats. Derived from a sister to Chriacus, Onychonycteris phylogenetically preceded Icaronycteris, Myotis and Pteropus in the LRT (subset Fig. 2).

Figure 3. 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.

Onychonycteris is smaller than Chriacus,
but the preserved portions of the skull and teeth are similar in proportion and morphology (Fig. 3). So… perhaps the proportions of the missing portion of the Chriacus skull are similar (fig. 1). More fossils will tell.

Veselka et al. 2010
concluded that O. finneyi may have been capable of echolocation.

By contrast, Simmons et al. 2010
argued that O. finneyi was probably not an echolocating bat.

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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.
Simmons NB, Seymour KL, Habersetzer J and Gunnell GF 2010. Inferring echolation in ancient bats. Nature 466: E8.
Veselka et al. (8 co-authors) 2010. A bony connection signals larygenal echolocation in bats.Nature 463: 939–942.

wiki/Onychonycteris

The ‘smallest megabat’, Balionycteris, enters the LRT

Yesterday we looked at how bats are able to
cling inverted to broad cave walls and narrow branches with their twisted feet.

Today we add
Balionycteris (Fig. 2), the ‘smallest megabat’ to the large reptile tree (LRT, 1670+ taxa, subset Fig. 1).

Figure 1. Subset of the LRT focusing on the resurrected clade Volitantia, including dermopterans, pangolins, bats and their extinct kin.

Not surprisingly
Balionycteris nests basal to two larger megabats (= fruit bats = flying foxes), Pteropus and Rousetta in the LRT. The megabat clade nests between two micro bats, extinct Icaronycteris and extant Rhinopoma, both of which have a long Chriacus-type free tail. Balionycteris does not share this trait, so I searched for a megabat with a long tail.

Such a bat exists in the long-tailed fruit bat (Notopteris macdonaldi ). As expected, it nests at the base of the megabits in the LRT. More on this transitional taxon soon.

Figure 2. Balionycteris hanging from both sides of a slender branch by laterally-twisted feet.

Balionycteris maculatus (originally Cynopterus Thomas 1893; Matschie 1899; 5-6cm in length) is the extant spotted-winged fruit bat, the smallest megabat and (for one day, yesterday) the most primitive one in the LRT (details above). It can be readily distinguished from other small species of Pteropodidae by a single pair of lower incisors, 2 pairs of upper molars, and by characteristic pale spots on wing membranes, particularly on digit joints.

Figure 3. Balionycteris skull. Note the short rostrum, as in related micro bats.

Like microbats, 
Balionycteris has short, broad wings and highly maneuverable flight. Balionycteris inhabits small cavities, but rarely cave entrances, and roosts singly, or in small groups. Note the premolars and molars have reduced cusps, convergent with edentates, whales, pangolins and other placental mammals.

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References
Matschie P 1899. Die Fledermäuse der Berliner Museums für Naturkunde. 1. Megachiroptera 72: 80.
Thomas O 1893. On some new Bornean mammalia. Ann. Nag. Nat. Hist., S.6 (65):341-347.

wiki/Pteropus
wiki/Archaeopteropus
wiki/Rousettus
wiki/Balionycteris

How bat feet turn laterally, then upside-down

Bats are inverted bipeds.
They hang by branches and cave walls by their feet. While inverted, bat forelimbs are folded away until needed for flight. The hind limbs frame membranes linking the laterally oriented legs to the medial tail. We looked at the origin of bats from non-volant ancestors earlier here, here and at several earlier links therein (also see Fig. 3).

Figure 1. Hind limbs and closeup of ankle of Cynopterus, an extant micro bat, from Digimorph.org. Colors and diagram elements added here. Unlike most mammals, the knees are often above the hips in bats.

Bat experts know this, but it  comes as news to me.
A closer examination of bat hindquarters (Fig. 1) reveals two axial twists that add up to a ~180º rotated hind limb for the micro bat Cynopterus. The ankle is capable of additional rotation.

1. The acetabulum axially rotates ~90º from ventrolateral to dorsolateral.
2. The femur axially rotates so the distal end is ~90º rotated from the proximal head (Fig. 2).
3. The tarsal centralia also rotate upon the tibiale (Fig. 1).

Figure 2. Two views of a bat femur animated to show typical untwisted orientation of femoral head as found in most mammals.

Axial torsion in proximal bones ultimately produces a pes
that is dorsal side up in flight in derived extant bats. Based on these twists, bat knees appear to bend backwards compared to other mammals.

Figure 3. The basal bat, Onychonycteris. The feet are smaller and the hind limbs are more gracile primitively, like those of the bat precursor, Chriacus in figure 3.

In the transitional basal bat
Onychonycteris, the hind limb appears to be laterally oriented with long gracile hind limbs and the dorsal side of the tiny pes likewise oriented laterally. If you think such tiny feet seem less capable of inverted clinging compared to the relatively big feet of Cynopterus (Fig. 1), you’re being observant. But long legs and small feet are primitive for bats. So is inverted bipedal hanging. What you’re seeing is a transitional phase.

Figure 4. Hypothetical bat ancestors arising from a sister to Chriacus, which may be a large late survivor of a smaller common ancestor. Imagine stem bat 3 and Onychonycteris pinching the branch they hang from with long legs acting like pliers, an idea that did not occur to me years ago when this was illustrated.

Rather than clinging to the same side of the twig (or cave wall)
the long legs and small feet of Onychonycteris acted more like tongs or pliers, pinching both sides of a branch medially between them. We also see this in primitive micro bats, like long-tailed Rhinopoma and primitive megabats, like Balionycteris (Fig. 5).

Figure 5. Balionycteris, the smallest megabat, hanging from both sides of a slender branch by laterally-twisted small feet.

Is there any new process on the bat pelvis that facilitates such adduction?
Yes. The pubis often develops a bump or rod, a prepubic process, analogous to the prepubis in pterosaurs. This process anchors muscles of femoral adduction.

Colugos and pangolins
also hang inverted from branches like that, with feet on both sides of a supporting branch.

The outgroup to bats in the LRT,
Chriacus, (Fig. 4) does not preserve evidence of long bone axial torsion (the mid-portion of the femur is not preserved). The acetabulum does not open dorsally.

Hanging upside-down
is something nearly all small arboreal mammals (e.g. squirrels, tree shrews, monkeys, tree opossums) can do facilitated by a flexible ankle that ensures the claws attach to the bark at any angle. Only bats and their immediate ancestors had such a firm toe grip while inverted they no longer needed their hands to grip. That freed the forelimbs to evolve into infant nurseries and parachute-like wings, not quite like those of birds and pterosaurs (Fig. 5), which were bipedal the conventional way: right side-up.

Figure 6. Click to enlarge. The origin of the pterosaur wing and the migration of the pteroid and preaxial carpal. A. Sphenodon. B. Huehuecuetzpalli. C. Cosesaurus. D. Sharovipteryx. E. Longisquama. F-H. Bergamodactylus.

The axial rotation of long limb bones is rare in tetrapods,
but it also can be seen in metacarpal 4 of Sharovipteryx, Longisquama and basal pterosaurs like Late Triassic Bergamodactylus (Fig. 6). That twist facilitates wing (finger 4) folding in the lateral plane of the wing (Peters 2002) rather than against the palm as in other tetrapods, including bats. Apparently the storage of long wings was just as important as the evolution of the long wings themselves in all volant tetrapods.

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References
Peters D 2002. A New Model for the Evolution of the Pterosaur Wing – with a twist. – Historical Biology 15: 277–301.
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/Onychonycteris

 

Mystacina: a walking, climbing, scraping micro-bat

The little New Zealand bat, Mystacina
(Figs. 1, 2), provides a living example for the earlier drop and hover hypothesis for the origin of bat flight. Most bats hang by their feet and observe what is below when they are not flying. This one, not so much.

Figure 4. The false vampire bat hovering before attacking a mouse in dry fallen leaves, listening to locate is prey. Flapping is key. Pre-bats were not gliders. Prebats flapped their parachute-like forelimbs.

Distinct from other bats,
Mystacina spends about thirty percent of its time on the ground on all fours (see YouTube video link below), wings folded, digit 2, the ventral one, reduced to a bumper.

Figure 2. Skeleton of Mystacina tuberculata from Digimorph.org and used with permission. The large head size is a derived trait. Note the two large incisors, used for scraping away burrows in soft hollow trees, co-copted by vampire bats to scrape away cattle skin.

The sharp incisor teeth
are used to scrape away soft tree interiors to create arboreal burrows. This trait is co-opted by related and sometimes terrestrial vampire bats to scrape away cattle skin to start  bleeding.

Figure 3 Mystacina skull from Digimorph.org and colorized here.

The propatagium is small
to aid in terrestrial locomotion. Mystacina has a large brain. A YouTube video (click to view) shows Mystacina in action.

Based on its performance,
and location, I wondered if Mystacina would be one of the most primitive of bats. It is not. So it may have reverted to a more primitive way of getting along (walking on all fours) after earlier achieving inverted bipedality and flight. Perhaps isolation on New Zealand as the only endemic mammal permitted this to happen.

Can you think of another set of animals
that reverted to quadrupedal locomotion after achieving flight? (Answer below).

FIgure 4. Subset of the LRT focusing on bats and kin including Mystacina. No, Mystacina does not nest at the base of all bats. Manis is the extant pangolin. Cynocephalus is the extant colugo or flying lemur.

Mystacina tuberculata (Gray 1843; 6-7cm snout-vent length) is the extant New Zealand lesser short-tailed bat. The tail extends beyong the uropatagia. It sometimes feeds on nectar with a long hairy tongue, but is considered omnivorous because it eats beetles and larvae. Today’s post was inspired by the discovery of a fossil relative from the Miocene of New Zealand, Vulcanops jennyworthyae.

Be wary of NatGeo.com stories
with headlines about burrowing bats. Mystacina bats burrow their way into the cores of rotting trees using their scraping incisors, a point missed by the author of the story from 2018, but cited by her in another online story here. Bats did not create small caves in the ground. At best they disturbed or ran into dense leaf litter to locate their prey.

Earlier we looked at the origin of large wings/hands
as holders of fruit hanging from trees (Fig. 5), either for the fruit itself or for the insects boring through it. This allows fruit bats and micro bats to have a phylogenetic common ancestor (Fig. 4 in clawed bats like Icaronycteris and Onychonycteris.

Figure 5. Pteropus and Caluromys compared in vivo and three views of their skulls. Caluromys is in the ancestry of bats and shows where they inherited their inverted posture.

Hanging upside down is something
many, if not all basal placentals did and do (Fig. 5). Those who don’t, like humans, horses and elephants, are derived. In contrast, bats rely only on their feet to hang upside down. The tail is no longer involved and disappears in some taxa.

Figure 6. GIF animation thought experiment on the origin and evolution of bats from a Ptilocercus-like omnivore. A change is warranted in this illustration. Abdominal membranes were probably present in pre-bats, extending from the torso to the fingers. These created a flapping steerable  parachute for bat decent to the leaf litter forest floor.

If you’re still wondering about
the other animals that reverted to a quadrupedal configuration after learning how to fly, think of the pterodactyloid-grade pterosaurs, which did so four times by convergence (Figs. 7, 8) according to the large pterosaur tree (LPT). Based on the extreme small size of hatchlings due to phylogenetic miniaturization at the genesis of these clades, these baby pterosaurs were probably relegated to clambering through dense, moist leaf litter until reaching a size that enabled flight without rapid desiccation due to a high surface-to-volume ratio.

Figure 7. Click to enlarge. The descendants of Sordes in the Dorygnathus clade and their two clades of pterodactyloid-grade descendants.

I have to say,
putting together these cladograms of vertebrates, pterosaurs and therapsids has taught me more about the theory of evolution and the way things work than dissecting a frog ever did in high school, or picking matrix off a fossil later on. Comparative anatomy gives one an appreciation and understanding of micro-evolution, not only what happened, but often why it happened over a wide range of taxa, some of which have never been compared to one another before.

Figure 8. Click to enlarge. The base of the Scaphognathia illustrating the size reduction that preceded the size increase in the transition from Scaphognathus to several later, larger “pterodactyloid”-grade clades.

By contrast,
the focus of paleontology textbooks seems to be showing chapter after chapter of skeletons, too often without making such distant comparisons with a freedom not often enough permitted in academia.

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References
Gray JE 1843. List of the Specimens of Mammalia in the Collection of the British Museum, George Woodfall and Son, London.

wiki/Mystacina
wiki/Vulcanops

New PBS Eons video on “When Bats Took Flight”

Well, they got the ‘when” kind of right.
Unfortunately, the PBS team had no idea how, who, or why bats took flight.

The following is my summary comment
buried deeper on the PBS YouTube page with each passing hour and day:

“With phylogenetic analysis based on traits we know the ancestors of bats back to jawless fish. Currently Zhangheotherium, a basal pangolin, and Chriacus are proximal outgroups to bats. (see link below). DNA fails too often in deep time experiments (e.g. Laurasiatheria: camels, whales, etc.)

“The best way to understand the genesis of bat flght is to compare it to the colugo, which leaps from its perch and glides for distance using membranes stretched between long limbs. These membranes were coopted from an extended marsupium, a place to keep newborns safe in these very basal placentals not far from their marsupial ancestors. Colugos, like many primitive placentals, also hang upside down, but with four very long limbs and small fingers.

“By contrast bats are inverted bipeds with membranes stretched between elongate fingers and short hind limbs. They don’t fly like birds and pterosaurs do. Instead they push pulses of air down with their huge parachute-like wings and huge pectoral muscles. When pre-bats hung inverted from low branches, they were able to survey the leaf litter below, ready to pounce on insects and worms rustling in the leaves on the ground. The distance could have started at 10cm, then extended to a meter, then 10 meters. So that is where hyper-acute hearing first developed.

“Instead of leaping from tree to tree, pre-bats dropped straight down onto their prey. To slow their fall, they flapped their large parachute-type hands. These became larger over time. Embryo bats with big hands recapitulate the evolution of bats. Leaf litter provided a soft landing for the tiny parachuting pre-bats, but over time flapping before crashing slowly turned into hovering for accuracy inches above the leaf litter before pouncing. Some bats still do this today. Over still more time, improved hovering became flight.

“After flight, returning to their inverted roost was so much safer, due to no more tree trunk climbing.”

More details, images and links here: https://pterosaurheresies.wordpress.com/2018/06/18/the-origin-and-evolution-of-bats-part-4-distance-vs-accuracy/

The origin of bats is by far the most popular topic
here at PterosaurHeresies. Use keyword [bats] in the box above to find out more.

Not that closely related to bats…

…even so, the resemblance
clearly shows what pre-bats were like (Fig. 1), and not by convergence. Caluromys (right) is the last of the marsupials, transitional to basal placentals. Bats, like Pteropus (left), are not too far from basal placentals.

Figure 1. Pteropus and Caluromys compared in vivo and three views of their skulls. Note the hourglass-shaped nasals, similar frontals, similar overall silhouettes and similar palates. Juvenile Caluromys has only two molars, the same number found in all members of the Carnivora and by convergence Pteropus. Other basal placentals retain 4 or 4 molars.

Caluromys is in the ancestry of bats
in the large reptile tree (LRT, 1272 taxa). Caluromys shows where bats inherited their signature inverted posture, even though that genus is several nodes away from Pteropus.

Since Caluromys is basal to all other placentals,
maybe bats aren’t the odd ones after all, for hanging inverted. It’s the primitive way to go.  All the other placentals that stopped hanging inverted are the derived ones.

We looked at the origin of bats
here and in earlier posts linked therein.

Dual origin of turtles and triple origin of whales abstracts

It used to be easier to get papers published.
The following are manuscripts independently published online without peer-review at the DavidPetersStudio.com website. http://www.davidpetersstudio.com/papers.htm

Better to put it out there this way
than to let this work remain suppressed. Hope this helps clarify issues.

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Peters D 2018a. The Dual Origin of Turtles from Pareiasaurs
PDF of manuscript and figures

The origin of turtles (traditional clade: Testudines) has been a vexing problem in paleontology. New light was shed with the description of Odontochelys, a transitional specimen with a plastron and teeth, but no carapace. Recent studies nested Owenetta (Late Permian), Eunotosaurus (Middle Permian) and Pappochelys (Middle Triassic) as turtle ancestors with teeth, but without a carapace or plastron. A wider gamut phylogenetic analysis of tetrapods nests Owenetta, Eunotosaurus and Pappochelys far from turtles and far apart from each other. Here dual turtle clades arise from a clade of stem turtle pareiasaurs. Bunostegos (Late Permian) and Elginia (Late Permian) give rise to dome/hard-shell turtles with late-surviving Niolamia (Eocene) at that base, inheriting its Baroque horned skull from Elginia. In parallel, Sclerosaurus (Middle Triassic) and Arganaceras (Late Permian) give rise to flat/soft-shell turtles with Odontochelys (Late Triassic) at that base. In all prior phylogenetic analyses taxon exclusion obscured these relationships. The present study also exposes a long-standing error. The traditional squamosal in turtles is here identified as the supratemporal. The actual squamosal remains anterior to the quadrate in all turtles, whether fused to the quadratojugal or not.

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Peters D 2018b. The Triple Origin of Whales
PDF of manuscript and figures

Workers presume the traditional whale clade, Cetacea, is monophyletic when they support a hypothesis of relationships for baleen whales (Mysticeti) rooted on stem members of the toothed whale clade (Odontoceti). Here a wider gamut phylogenetic analysis recovers Archaeoceti + Odontoceti far apart from Mysticeti and right whales apart from other mysticetes. The three whale clades had semi-aquatic ancestors with four limbs. The clade Odontoceti arises from a lineage that includes archaeocetids, pakicetids, tenrecs, elephant shrews and anagalids: all predators. The clade Mysticeti arises from a lineage that includes desmostylians, anthracobunids, cambaytheres, hippos and mesonychids: none predators. Right whales are derived from a sister to Desmostylus. Other mysticetes arise from a sister to the RBCM specimen attributed to Behemotops. Basal mysticetes include Caperea (for right whales) and Miocaperea (for all other mysticetes). Cetotheres are not related to aetiocetids. Whales and hippos are not related to artiodactyls. Rather the artiodactyl-type ankle found in basal archaeocetes is also found in the tenrec/odontocete clade. Former mesonychids, Sinonyx and Andrewsarchus, nest close to tenrecs. These are novel observations and hypotheses of mammal interrelationships based on morphology and a wide gamut taxon list that includes relevant taxa that prior studies ignored. Here some taxa are tested together for the first time, so they nest together for the first time.

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Both of these manuscripts benefit from
ongoing studies at the large reptile tree (LRT, 1247 taxa) in which taxon exclusion possibilities are minimized and all included taxa can trace their ancestry back to Devonian tetrapods.

YouTube video supports newest bat origin hypothesis

Figure 1. The false vampire bat hovering before attacking a mouse in dry fallen leaves, listening to locate is prey in accord with a hypothesis of bat origins first presented here. The first pre-bats were not as adept at falling on prey, but refinements followed.

Earlier we looked at a new hypothesis for bat origins
that separated the distance gliding origins of small-hand colugos from the accurate falling, flapping origin of big-hand bats. Today readers get to see a video (below, Figs. 1, 2) showing that ancient and original behavior – still retained by the carnivorous wooly false vampire bat (genus: Chrotopterus). This may not be the most primitive extant bat, but this video demonstrates the predatory behavior that led to the origin of bats:

1. inverted hanging >
2. falling on prey while flapping to brake its descent >
3. covering the prey item with ankle-to-hand membranes >
4. capturing the prey item with its mouth >
5. leaving the scene of the attack with prey in tow to feed later.

Figure 2. Scenes from the video showing the stages in the bat attack on the mouse in the leaf litter. Note how the former nursery membrane, now a flight membrane, covers the prey, preventing its escape.

Click the video to view it.

Before bats had sonar
bats relied on rustling sounds in the leaf litter to find their rodent and insect prey. Gradually refining this ability is what led to sonar in micro bats.

Before bats could fly
inverted pre-bats fell from tree limbs, flapping their small hands to slow their inevitable descent. Gradually refining this ability, while gradually enlarging those big membraned bat hands is what led to slowing the decent, hovering prior to the attack and ultimately flying and chasing flying insect prey.

This bat origin hypothesis
solves the problem of bat flapping without display (as in theropods and fenestrasaurs) and without WAIR (wing-assisted inclined running, as in theropods and fenestrasaurs). Remember bats have very weak and rotated backwards hind feet. Bipeds they were, but inverted and non-cursorial, distinct from pterosaurs and birds.

Remember
colugos, bats and basal pangolins, like Zhangheotherium, were members of the clade Volitantia. This placental clade is close to metatherian stem placentals, like Monodelphis, that have ventrally open pouches. These pouches were originally to protect nursing underdeveloped newborns, then expanded to form nursery membranes, then further expanded and co-opted for gliding in colugos and flying in bats.

How wonderful
that some bats retain their original and ancient method of hunting, as shown in the video. So many times in paleo, the answer has been staring at us, out in the open, waiting for recognition. On that note, I have sent emails to several leading bat experts, referring them to the earlier blogpost on bat origins, asking for their feedback. None, so far, have responded.

References
photographer: Anand Varma

wiki/Chrotopterus

The origin and evolution of bats part 4: distance vs. accuracy

Earlier
we looked at bat origins here, here and here from several perspectives. Some of these are now invalid given the following scenario.

Today we’ll take a fresh look at
the behavior and traits of the closest bat relatives in the large reptile tree (LRT, 1233 taxa, subset Fig. 1) and see what they can tell us about bat origins. This is called ‘phylogenetic bracketing‘. In such a thought experiment we can put forth an educated guess regarding an unknown behavior or trait for a unknown taxa (e.g. pre-bats) if all related specimens share similar behaviors and traits inherited from a known or unknown last common ancestor.

We start off with a cladogram
focusing on bat relationships (Fig. 1) and take things one logical step at a time.

Figure 1. Subset of the LRT focusing on basal placentals, including bats.

One. Living sister taxa.
The closest tested sister taxa to bats here (Fig. 1) are pangolins and colugos (flying lemurs) in order of increasing distance. The origin of bats and pangolins has remained a traditional enigma. Like the origin of pterosaurs and Longisquama, the surprise is, they are most closely related to each other, despite their current differences.

Two. Ancestral taxa
Th bat/colugo/pangolin clade had its genesis near the original dichotomy of placental mammals, when Carnivora split off from all others. At the next dichotomy the bat/colugo/pangolin clade split off from all others. So this clade is not far from an ancestral clades with living genera. Monodelphis, the short-tailed opossum today restricted to South America, nests just outside of all mammals with a placenta. Nandinia, the African palm civet, is a basal member of the Carnivora, somewhat larger than its Mesozoic forebearers.

Three. Timing for clade origins
The bat/colugo/pangolin clade had its origin in the Early Jurassic based on the more primitive egg-layers, Megazostrodon, Brasilitherium and Kuehneotherium in the Late Triassic and the much more derived arboreal multituberculate/rodent, Megaconus, in the Middle Jurassic. As you can see, Jurassic mammals remain extremely rare, currently represented only by the likes of Megaconus. Others will, no doubt, be discovered in time.

Four. Arboreality (tree niche)
Some bats, colugos and pangolins live in trees, and so do their last common ancestors, short-tailed opossums and African palm civets.

Five. Climbing trees
Bats no longer have to climb trees because they can fly. Colugos and pangolins both climb trees in a series of symmetrical short hops/extended reaches (colugo video, pangolin video), distinct from palm civets and short-tailed opossums, which put forth one hand at a time, like primates do.

Six. Descending trees.
Bats fly between trees. Colugos glide between trees. Pangolins use their prehensile tail to ease themselves down. The African palm civet drops out of trees in play. It also descends tree trunks like a squirrel, head first.

Seven. Nocturnal
Most bats, colugos, pangolins, palm civets and short-tailed opossums prefer to be active at night.

Eight. Omnivorous diet
Some bats eat insects, others prefer nectar or hanging fruit. Colugos prefer leaves, shoots, flowers, sap, and fruit. Pangolins eat ants. Palm civets and short-tailed opossums are omnivorous. African palm civets feed by holding their prey in their hand-like front paws, biting it repeatedly and then once dead, swallowing it whole.

Nine. Extradermal membranes
Colugos and bats both have extradermal membranes to their unguals that extend their glides in the former and enable flapping flying in the latter. Such membranes are lost in living pangolins, but the Early Cretaceous pangolin, Zhangheotherium appears to have scale-lined membranes between the elbows and knees. These were overlooked in the original description. The gliding membrane in colugos is fur-covered and camouflaged dorsally, naked underneath. In bats the flying membrane is naked, translucent and never camouflaged.

Ten. Mobile clavicle, interclavicle and scapula
The basal pangolin, Zhangheotherium, has a mobile clavicle-interclavicle and the large scapula rises above the  dorsal vertebrae, as in bats, but not colugos.

11. Sprawling femora
Zhangeotherium and bats share sprawling hind limbs, distinct from the more erect hind limbs of most limbed mammals.

12. Silent vs. noisy
African palm civets are noisy. Colugos and pangolins are largely silent. Bats are constantly chirping to one another and (micro-bats only) as part of their sonar attack system.

13. Enemies
All current enemies of bats (e.g. birds, snakes) evolved during or after the Late Cretaceous. Jurassic trees might have been a refuge for small early climbing mammals, like colugo, bat and pangolin ancestors. However…the minimally feathered, small theropod dinosaur, Sinosauropteryx, contained the jaws of Zhangheotherium, perhaps caught after descending from the trees or plucked out of lower branches. Certain pterosaurs (e.g. giant anurognathids) might have preyed on arboreal  mammals in the Jurassic, but no evidence of this is yet known.

FIgure 2. Calcaneal spur in Zhangheotherium. Not venomous, but perhaps to anchor a uropatagium as in bats.

14. Calcaneal spurs
Hurum et al. 2006 originally considered the small spurs found on the calcaneum of Zhangheotherium (Fig. 2) similar to venom spurs found on the platypus, Ornithorhynchus. Phylogenetic bracketing indicates the closer homolog is with the basal bat, Onychonycteris, which has longer calcaneal spurs framing a trailing uropatagium.

Figure 3 Monodelphis babies in an open pouch. This is how placentals began, slowly evolving from the less open pouch.

15. Newborns and mothers
All basal placental mammals give birth to helpless newborns that ride with the mother until mature enough to go out on its own. Monodelphis demonstrates a primitive version of this, protecting its ten young with lateral flaps of skin (Fig. 3). Carnivore mothers make nests for newborns (2-4 for African palm civets), but colugo, bat and pangolin mothers take their one or two babies everywhere they go, like marsupial mothers do. Zhangheotherium might have been fossilized with several newborns. (Fig. 4) and extradermal membranes between elbows and knees, as in bats and colugos. As we know from colugos, these extradermal membranes in basal pangolins (and Chriacus?) likely formed a playpen or nursery for developing young riding beneath their mother during the earliest stages of development.

Figure 4. Zhangheotherium showing possible extradermal membranes (light blue and green) with keratinous scales (red) and several newborns scattered in the abdominal area, similar to Monodelphis in figure x. These amorphous blobs with tiny tail bones need further inspection. Some may just be stains and shapes.

16. Curling (flexing the spine)
Mother opossums, palm civets, colugos, bats and pangolins are able to curl their spines so much that the mother’s mouth is able to assist wiggling newborns climb to the abdominal nipples. This curling ability is co-opted by pangolins as they defend themselves by rolling into a tight ball and by bats that catch prey in their tail before curling up to bite the victim as it is brought close to the jaws. Higher mammals lose the ability to curl ventrally in this manner. Humans and other primates have a limited ability to do this. Instead they use their hands. More derived mammals with stiffer backs have more developed newborns.

17. Upside-down vs. right-side up nursery for the young
Colugos may rest right-side up (preferring to hang from below a slightly leaning tree trunk) or upside down hanging by all fours beneath a horizontal branch. When doing so the mother’s extradermal membranes form walls making a protective nursery for the young ones.

By contrast, bats rest up-side down, sometimes hanging by only one locked foot. To fly bats simply release this foot lock, then plummet and start flapping. Bat membranes also provide a protective nursery for their young as they cling to their mothers’ chest and her wings fold over them.

Nowadays pangolins roll into a ball while nursing their young. Later in life, babies ride on the mother’s back and tail when able to do so. Zhangheotherium (Fig. 4) appears to have provided a colugo-like, but scale-lined membrane nursery for several growing babies. The late-surviving pre-bat, Chriacus (Fig. 5), likely did the same, based on phylogenetic bracketing.

18. Claws
Short-tailed opossums and African palm civets use their claws to climb trees and grab prey and fruit, bringing it to the mouth. So do basal primates. Colugos, bats and pangolins use their larger, curved claws principally to hang from trees, though living pangolins have co-opted their large claws to dig out ant and termite nests from trees and underground.

19. Distance vs. accuracy
Colugos leap and turn away from their tree trunk base in order to launch themselves into a glide. Can they do this while hanging beneath a branch? I don’t know. With their long limbs, colugos can just leap (without gliding) across gaps of 5m or more. With limbs extended, they can glide for 136m at 10m/second. Gliding is good for a quick escape from predators, and access to patches of food that are otherwise inaccessible. It does not save them energy to glide, let along climb back to a gliding height.

Bats drop from trees, then fly wherever they please, typically landing upside down on another high branch or cavern roof. The origin of bat flight enabled by flapping hyper-elongated webbed fingers is the key question here, and it is answered by combining all of the above numbered traits.

Before bats could fly Jurassic pre-bats had to climb trees, probably like colugos and pangolins do (see #5 above), before standing bipedally, but upside-down, on a horizontal branch. Why would they do that? To prepare to dive bomb insects on and in the leaf litter below. Here is where sonar became valuable, detecting insects in the leaf litter at night. Here is where the leaf litter became valuable, cushioning the early awkward landings of small dive-bombing pre-bats. Here is where flapping, even with small hands around colugo-like dermal membranes became valuable, at first in panic, then in gradually learning how to better direct the fall to cover the prey below.  (By analogy birds flap their wings vigorously while dropping to slow their descent.)

Upon landing the extended pre-bat nursery membranes ‘put a lid’ on the prey. Then, curling the tooth-line jaws toward the tail and the tail toward the jaws (see #16 above) spelled doom for the captured food item. Over time, larger fingers made better flapping parachutes. Ultimately flapping bats  learned how to hover before diving bombing their prey, like owls do. Later, after further development, bats gained the power and morphology to enable flight, slowly at first, then better and better to escape ground-dwelling predators and avoid having to climb a tree for the next attack. Only later did bats learn to use their sonar and flying skills on flying insects.

So what began as a small pouch, then a larger nursery membrane for bat and colugo infants became a killing zone for bat prey on the ground, another example of co-opting an old trait for a new behavior in derived taxa. Distinct from birds and pterosaurs, which used their nascent flapping behavior to ascend tree trunks to escape predators, create threat displays and slow their descents from branches, bats used their nascent flapping ability only to slow and direct their descent from branches. Distinct from colugos, which glided for distance, bats dropped for accuracy. Distance came later, after flight developed.

Remember the fall need not be far at first. Conifers can have very low branches and leaf litter can be a soft cushion for a mouse-sized mammal. Graduating slowly to higher branches provides bats a wider ‘field-of-view’ for their slowly developing sonar, and more time to develop flapping. Bat hind limbs are not long or heavily muscled. They are not good at leaping, like colugos.

Fruit eating bats could not have developed until flowering and fruit-bearing trees developed, later in the Cretaceous. The LRT and the fossil record indicates that fruit-eating bats are derived relative to smaller insect-eating bats. So sonar-emitting apparently was lost in fruit-eating bats, rather than never a part of their lineage. The great variation now seen in sonar-emitting bat morphology was likely developed during and after the Cretaceous, based on the current fossil record. I think we’ll find fully volant fossil bats in the Cretaceous someday.

I happened upon this idea while watching a pigeon descend from a roofline to a balcony beneath it and wondered if accuracy was more important for bats, while distance was more important for colugos. That distinction seems to be the key driver in both clades. In any case, it is important that any proposed scenario be viable at every point during the gradual evolution of new traits and behaviors. In this case, developing flapping forelimbs had to originate with a bipedal configuration, even it inverted. Developing sonar had to originate from simply listening to nocturnal insects and other small prey rustling in the leaf litter, not far below, gradually getting better in those families that randomly had slightly better skills once dive-bombing and trapping became the method for predation.

20. Bat ontogeny
Recapitulates this phylogenetic scenario. The fingers elongate last. 

21. Solitary vs. communal
Colugos and pangolins are solitary. So are African palm civets except when food is plentiful. Bats are communal, whether nesting in trees or caves. According to Kerth 2008, “Variable dispersal patterns, complex olfactory and acoustic communication, flexible context-related interactions, striking cooperative behaviors, and cryptic colony structures in the form of fission-fusion systems have been documented. tropical bats often form groups year-round, whereas sociality in temperate-zone species is sometimes restricted to certain times of the year. In most species, females form so-called maternity colonies to rear their young communally, whereas males are solitary, form groups of their own, or join female groups. In only a few species are both sexes solitary, meeting only to mate.”

Kerth concludes, “None of the three factors that I identify as important for the evolution of sociality in bats (ecological constraints, physiological demands, and demographic traits) can fully explain the frequency and diversity of group living in bats.”

Figure 5. Basal placentals at two scales, all arising from a Middle Jurassic sister to Monodelphis, based on the Earliest Cretaceous appearance of Zhangheotherium, in the lineage of pangolins..

22. Soles of the feet oriented opposite to those of most mammals
Distinct from most mammals, the knees of bats are splayed laterally, which should extend the toes laterally. However, the ankle is rotated another 90º producing a foot in which the soles are ventral during flight and while hanging. In the case of long-legged fish-eating bats, the feet help bring captured fish back to the mouth.

FIgure 6. Wondering if Chriacus had an inverted stance and dermopteran membranes? Comparisons to Onychonycteris and Pteropus are shown. Yes, the knees are straight in derived fruit bats, bent in Onychonycteris and micro bats. The uropatagia are spread while inverted and while flying. Chriacus appears to be a much larger and much later-surviving version of much smaller Jurassic pre-bats. The membranes are conjectural and may have been lost in this large specimen, but it illustrates the possibility of a dive bombing taxon that covered prey like a casserole lid.

Why do bats hang upside down?
Without a phylogenetic or deep-time perspective, the following video is the best answer current bat workers can provide:

Bats are not using their wings to cool off.
A recent heat wave killed many fruit bats. They fell dead out of the trees (see below). None were creating a cooling breeze with their wings or extending their wings in a cooling fashion, like elephants sometimes do. Microbats that live in caves never have this problem.

Bat wings notes:

1. Finger flexibility during flight varies greatly in bats.
2. The flight stroke is otherwise bird-like with elbows raised above the back, nearly meeting at the midline, for maximum power at low airspeed, or less so for cruising at higher airspeeds.
3. The large fingers do nothing else but push air for thrust and lift. They are not extended to cool the bat, nor do they extend or flash during courtship.
4. Bat fingers hyper flex at the wrist to tuck away the flight membrane and reduce its surface area when not in use, as in pterosaurs and birds. When flexed they do little but envelope the bat and its clinging young.

Miscellaneous notes:

1. Zhangheotherium was originally considered a symmetrodont mammal, but its teeth seems to converge with archaeocete whales in this regard. The reappearance of a more primitive symmetrodont molar shape is here considered an atavism in the evolution of toothlessness in both certain odontocetes and pangolins by convergence.
2. The uncoiled cochlea of highly derived Zhangheotherium and multituberculates, has been traditionally considered a trait that nests these taxa in more basal branches of the mammal family tree. Here, in the LRT, these traits appear to be neotonous or atavistic developments that, taken alone, tend to confuse systematics. No traits should ever be taken alone to determine systematics. That would be ‘pulling a Larry Martin.’
3. The initial splitting up of Pangaea in the Early Jurassic gave the previously dry climate a more lush, subtropical parade of cycads, conifers, ginkgoes and tree ferns. So there were plenty of standing and fallen trees for early mammals to gambol upon, learning how to climb and leap. The forest floor was likely cushioned with a carpet of leaves and fronds to absorb accidental falls and hunger-driven dive bombs mediated by fluttering pre-wings and large membranes co-opted for eventual flight.

Addendum
Video showing a bat descending on a mouse in leaf litter appears here.

References
Byrnes, Libby, Lim & Spence. 2011. Gliding saves time but not energy in Malayan colugos. Journal of Experimental Biology http://dx.doi.org/10.1242/jeb.052993
Hurum JH, Luo Z-X and Kielan-Jaworowska Z 2006. Were mammals originally venomous? Acta Palaeontologica Polonica 51(1): 1–11.
Kerth G 2008. Causes and Consequences of Sociality in Bats. BioScience, Volume 58, Issue 8, 1 September 2008, Pages 737–746, https://doi.org/10.1641/B580810
Online here.