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Again, reading from outdated textbooks,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. IPteropodidae (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.

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 to scale. Click to enlarge.

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 Onychonycteris, a basal bat.

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.


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.

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

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 ChriacusOnychonycteris phylogenetically preceded IcaronycterisMyotis and Pteropus in the LRT (subset Fig. 2).

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 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.


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

Two primitive extant bats enter the LRT

Yesterday we looked at the smallest of the fruit bats (mega bats). Earlier we looked at several micro bats.

Here, at nearly the same size,
Notopteris (Figs. 1, 2( nests in the large reptile tree (LRT, 1671+ taxa, subset Fig. 5) as the most primitive extant megabat due to its long tail and a few other primitive traits.

Figure 1. Notopteris in vivo. Note the microbat proportions and relatively long tail. The wing membrane begins along a dorsal margin, not laterally as in other bats.

Figure 1. Notopteris in vivo. Note the microbat proportions and relatively long tail. The wing membrane begins along a dorsal margin, not laterally as in other bats.

Notopteris macdonaldi (Gray 1859) is the long-tailed fruit bat or Fijian blossom bat. This is the most primitive megabat in the LRT and the only one that retains a long tail. It roosts in large cave colonies only on South Pacific islands. Note the mid-dorsal attachment of the proximal wing membranes, rather than a more lateral attachment. This is a derived trait not shared with other bats.

Figure 2. Notopteris skull and mandible.

Figure 2. Notopteris skull and mandible. Note the primitive skull and derived simple cusp teeth.

The most primitive extant microbat
in the LRT (Figs. 3, 4) is the newly added Rhinopoma, the lesser mouse-tailed bat (Fig. 3). It is similar, to Notopteris (Figs. 1, 2), but with a shorter rostrum and retains primitive multiple cusps on its teeth. Both are cave dwellers.

Figure 3. Rhinopoma is the most primitive extant micro bat in the LRT. Note the long tail, long legs and small feet, all Chriacus-like and Onychonycteris-like primitive traits.

Figure 3. Rhinopoma is the most primitive extant micro bat in the LRT. Note the long tail, long legs and small feet, all Chriacus-like and Onychonycteris-like primitive traits. Note the lateral insertion of the wing membrane on the torso, distinct from Notopteris (Fig. 1).

Rhinopoma hardwickei (Gray 1831) is the extant lesser mouse-tailed bat, an insectivore found from North Africa to India. The tail is 3/4 free and no calcar is present on the heel. The legs are long and the feet are small.

Figure 4. Rhinopoma skull from Digimorph.org and used with permission.

Figure 4. Rhinopoma skull from Digimorph.org and used with permission. Note the prominent ear bones (yellow) in this echolocating microbat.

Simmons et al. 1984 looked at echolocation in Rhinopoma.
They concluded, “Except for duration these signals are relatively inflexible and suggestive of a primitive kind of echolocation in which only one dimension is changed to achieve qualities which most other species of bats obtain by changing a variety of signal dimensions simultaneously.”

Nelson and Hamilton Smith 1982 looked at echolocation in Notopteris.
They concluded, “Some field experiments… showed these flying foxes were unable to avoid obstacles in complete darkness or when blindfolded, but were able to do so in very dim light. No audible or ultrasonic sounds that could be used in echolocation were detected during their flight.”

Holland et al. 2004 looked at echolocation in the megabat Rousettus.
They reported, “Rousettus aegyptiacus Geoffroy 1810 is a member of the only genus of Megachiropteran bats to use vocal echolocation, but the structure of its brief, click-like signal is poorly described.Rousettus aegyptiacus Geoffroy 1810 is a member of the only genus of Megachiropteran bats to use vocal echolocation, but the structure of its brief, click-like signal is poorly described. However, the low energy content of the signals and short duration should make returning echoes difficult to detect. The performance of R. aegyptiacus in obstacle avoidance experiments using echolocation therefore remains something of a conundrum.”

Simmons and Geisler 1998 looked at echolocation in Icaronycteris.
They reported, “We propose that flight evolved before echolocation, and that the first bats used vision for orientation in their arboreal/aerial environment. The evolution of flight was followed by the origin of low-duty-cycle laryngeal echolocation in early members of the microchiropteran lineage. This system was most likely simple at first, permitting orientation and obstacle detection but not detection or tracking of airborne prey.”

Veselka et al. 2010 concluded that Onychonycteris finneyi may have been capable of echolocation. in reply, Simmons et al. 2010 argued that Onychonycteris finneyi was probably not an echolocating bat.

Echolocation seems to have been convergently acquired
in microbats and Rousettus.

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

Figure 5. Subset of the LRT focusing on the resurrected clade Volitantia, including dermopterans, pangolins, bats and their extinct kin.

Basal bats in the LRT have more plesiomorphic traits overall,
like small ears, simple nose, long legs, long tail and small feet, all Chriacus-like (Fig. 6) traits. This is what we should expect when any cladogram models micro-evolutionary changes.

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 6. 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.

We looked at the origin of bats from Chriacus-like ancestors
earlier here, here and at earlier links therein. These posts are –by far– the most popular posts at this PterosaurHeresies.

To summarize one of those posts
hanging pre-bats simply listened for the sounds of prey in leaf litter below, then pounced from above. Parachuting with flapping evolved into helicoptering then that evolved into flight to return to the branch the bat fell from. Larger hands and extradermal membranes would have increasingly aided entrapment at the moment of impact. Even larger hands and extradermal membranes would have increasingly helped helicoptering while falling. Smaller size and weight (Fig. 6) was co-opted to aid these behaviors. Echolocation seems to have evolved in bats seeking aerial prey and co-opted to live in caves in complete darkness.


References
Gray JE 1831. Description of some new genera and species of bats. The Zoological Miscellany, 1: 37-38.
Gray GR 1859.
 The annals and magazine of Natural History, Zoology, Botany and Geology 3. Series IV: 4859.
Holland RA, Waters DA and Rayner JMV 2004. Echolocation signal structure in the megachiropteran bat Rousettus aegyptiacus Geoffroy 1810. Journal of Experimental Biology 207:4361–4369.
Nelson JE and Hamilton-Smith E 1982. Some observations on Notopteris macdonaldi (Chiroptera: Pteropodidae) in Australian Mammal Society 5: 247–252.
Simmons JA, Kick SA and Lawrence BD 1984. Echolocation and hearing in the mouse-tailed bat, Rhinopoma hardwickei: acoustic evolution of echolocation in bats. Journal of Comparative Physiology A 154: 347–356.
Simmons NB and Geisler JH 1998. Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation. Bulletin of the American Museum of Natural History 235.
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/Notopteris

wiki/Rhinopoma

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.

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

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

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.


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.

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. Bat femur animated to show untwisted typical mammal orientation of femoral head.

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.

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

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

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.


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 1. The false vampire bat hovering before attacking a mouse in dry fallen leaves, listening to locate is prey.

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 1. Skeleton of Mystacina tuberculata from Digimorph.org and used with permission. The large head size is a derived trait.

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 2. Mystacina skull from Digimorph.org and colorized here.

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 3. Subset of the LRT focusing on bats and kin including Mystacina.

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 1. 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.

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

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

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.

The base of the Scaphognathia

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.


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 ground effect study supports origin of bat flight hypothesis proposed here

A new paper by Johansson, Jakobsen and Hendenstram 2018
introduces the benefit of ground effect (the surface acts as an aerodynamic mirror, interrupting the downwash, resulting in increased pressure underneath the wing and suppression of wingtip vortex development) in the origin of bat flight.

This is something every student pilot learns.
Ground effect is basic aerodynamics whether applied to bats, airplanes or flying fish.

Figure 1. The false vampire bat hovering before attacking a mouse in dry fallen leaves, listening to locate is prey.

Figure 1. The false vampire bat hovering before attacking a mouse in dry fallen leaves, listening to locate is prey.

Even so, it is measured here for bats for the first time.
You might remember, an earlier hypothesis first published here proposed an origin of bat flight associated with dropping out of trees while frantically flapping to break the fall in order to attack insects heard in the leaf litter (Fig. 1). The benefit of such unprofessional flapping increases as the ground gets closer and closer. In bats this frantic flapping while parachuting evolved to hovering before ground contact (with the help of ground effect). And this evolved to powered flight in bat-fashion, distinct from bird and pterosaur flight origins.

Highlights of the Johansson, Jakobsen and Hendenstram 2018 paper:

  1. Aerodynamic power is 29% lower when bats fly close to rather than far from ground
  2. Measured savings are twice the savings expected from models
  3. Wing motion is varied with distance to ground, which may modulate ground effect
  4. The results challenge our understanding of how animals use ground effect

References:
Johansson LC, Jakobsen L and Hendenstram A 2018. Flight in ground effect dramatically reduces aerodynamic costs in bats. Current Biology. DOI: https://doi.org/10.1016/j.cub.2018.09.011
https://www.cell.com/current-biology/fulltext/S0960-9822(18)31206-5

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. Caluromys is in the ancestry of bats and shows where they inherited their inverted posture.

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.


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.


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.


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.

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.

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