Heers et al. 2021 discuss the origin of flight using hatchling birds

Short one today
as Heers et al. 2021 miss the one key trait in the evolution of flapping flight in bird origins: a locked-down elongate coracoid necessary for left-right simultaneous flapping. This morphology is derived from the primitive disc-like coracoid sliding on the sternal rim, originally used during quadrupedal locomotion to extend each stride (Fig. 1). Disc-like coracoids are retained in bipedal theropods like TyrannosaurusKhaan, and Haplocheirus.

The coracoids (in pink)

Figure 1. The coracoids (in pink) slide along the sternum behind the interclavicle.

By contrast
in Velociraptor, Archaeopteryx and living birds the coracoid is no longer mobile and disc-like, but narrows and becomes immobile. These are flapping bipeds. This fact was overlooked by Heers et al. who looked a baby birds.

Figure 3. The Eichstätt specimen, Jurapteryx recurva, nests with the living ostrich, Struthio, presently in the LRT.

Figure 2. The Eichstätt specimen, Jurapteryx recurva, nests with the living ostrich, Struthio, presently in the LRT.

From the Heers et al. abstract:
“Although extinct theropods are most often compared to adult birds, studies show that developing birds can uniquely address certain challenges and provide powerful insights into the evolution of avian flight: unlike adults, immature birds have rudimentary, somewhat “dinosaur-like” flight apparatuses and can reveal relationships between form, function, performance, and behavior during flightless to flight-capable transitions. Here, we focus on the musculoskeletal apparatus and use CT scans coupled with a three-dimensional musculoskeletal modeling approach to analyze how ontogenetic changes in skeletal anatomy influence muscle size, leverage, orientation, and corresponding function during the development of flight in a precocial ground bird (Alectoris chukar).”

Unfortunately, even baby birds have a locked-down elongate coracoid. So the transition to flapping must be found in the fossil record, not the ontogeny of chicks. Heers et al. needed an outgroup and a convergent set of taxa.

Figure 1. Cosesaurus flapping - fast. There should be a difference in the two speeds. If not, apologies. Also, there should be some bounce in the tail and neck, but that would involve more effort and physics.

Figure 3. Click to enlarge and animate. Cosesaurus flapping – fast. There should be a difference in the two speeds. If not, apologies. Also, there should be some bounce in the tail and neck, but that would involve more effort and physics.

Figure 2. Cosesaurus torso and forelimbs. The hot pink stem-like coracoids are found in pterosaurs. So are the strap-like scapula, distinct from the discs found in Macrocnemus. There is a close association of the clavicles, interclavicle and sternum. In pterosaurs this is known as a sternal complex.

Figure 4. Cosesaurus torso and forelimbs. The hot pink stem-like coracoids are found in pterosaurs. So are the strap-like scapula, distinct from the discs found in Macrocnemus. There is a close association of the clavicles, interclavicle and sternum. In pterosaurs this is known as a sternal complex.

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

Figure 5. Ptilcercus (above) and Icaronycteris (below), sister taxa in the origin of bats.

starting with Cosesaurus (Figs. 3, 4) had bird-like immobile coracoids.

(Fig. 5) don’t have coracoids. but elongate locked-down clavicles are analogous.

Heers AM, Varghese SL, Hatier LK and Cabrera JJ 2021. Multiple Functional Solutions During Flightless to Flight-Capable Transitions

Locked down coracoid discussion

150 million years of pterosaur flight efficiency

Venditti et al. 2020
attempts to chronicle an increase in pterosaur flight efficiency over their 150 million year long clade span.

From the Venditti et al. abstract:
“The long-term accumulation of biodiversity has been punctuated by remarkable evolutionary transitions that allowed organisms to exploit new ecological opportunities. Mesozoic flying reptiles (the pterosaurs), which dominated the skies for more than 150 million years, were the product of one such transition. The ancestors of pterosaurs were small and probably bipedal early archosaurs (Andres et al. 2014), which were certainly well-adapted to terrestrial locomotion.”

Citation and taxon exclusion here. Andres et al. 2014 cherry-picked four euarchosauriform outgroups for the Pterosauria: Euparkeria, Ornithosuchus, Herrerasaurus and Scleromochlus. All of these taxa have a short to vestigial manual digit 4, the opposite of pterosaurs. This list followed the direction of co-author Mike Benton, well known for citation and taxon exclusion to promote his pet hypotheses, invalidated by Peters 2000, 2007, 2009. Readers have seen Benton omissions many times. The actual ancestors of pterosaurs were not archosaurs, but these lepidosaurs: Cosesaurus (Fig. 1), Sharovipteryx and Longisquama. So Venditti et al. 2020 starts off poorly, without a proper phylogenetic context.

By the way, Andres et al.  2014 did not find ‘the earliest pterodactyloid,’ but bits and pieces of a gracile dorygnathid, Sericipterus found in the same formation.

Figure 1. Cosesaurus flapping - fast. There should be a difference in the two speeds. If not, apologies. Also, there should be some bounce in the tail and neck, but that would involve more effort and physics.

Figure 1. Click to enlarge and animate. Cosesaurus flapping – fast. There should be a difference in the two speeds. If not, apologies. Also, there should be some bounce in the tail and neck, but that would involve more effort and physics.

Continuing from the Venditti et al. abstract:
“Pterosaurs diverged from dinosaur ancestors in the Early Triassic epoch (around 245 million years ago); however, the first fossils of pterosaurs are dated to 25 million years later, in the Late Triassic epoch.”

False: Pterosaurs diverged from fenestrasaur ancestors (Peters 2000).

“Therefore, in the absence of proto-pterosaur fossils, it is difficult to study how flight first evolved in this group.”

False. We have those proto-pterosaur fossils and pterosaur ancestors all the way back to Cambrian chordates. Adding taxa resolved this problem in Peters 2000, 2007, 2009 and that continues today.

“Here we describe the evolutionary dynamics of the adaptation of pterosaurs to a new method of locomotion. The earliest known pterosaurs took flight and subsequently appear to have become capable and efficient flyers. However, it seems clear that transitioning between forms of locomotion2,3—from terrestrial to volant—challenged early pterosaurs by imposing a high energetic burden, thus requiring flight to provide some offsetting fitness benefits.”

Or the other way around, as documented by the four fenestrasaurs listed above.

“Using phylogenetic statistical methods and biophysical models combined with information from the fossil record, we detect an evolutionary signal of natural selection that acted to increase flight efficiency over millions of years.”

What is ‘flight efficiency’? Are hummingbirds more efficient? Or are albatrosses? Or ducks? Did the authors use the proper pterosaur wing shape (Fig. 2) ? Or the traditional invalid batwing-shape preferred by those in the Benton arc.

The Vienna Pterodactylus.

Figure 2. The Vienna Pterodactylus. Click to animate. Wing membranes in situ (when folded) then animated to extend them. There is no shrinkage here or in ANY pterosaur wing membrane. There is only an “explanation” to avoid dealing with the hard evidence here and elsewhere.

“Our results show that there was still considerable room for improvement in terms of efficiency after the appearance of flight.”

Without valid outgroups, how do they know? They don’t.

“However, in the Azhdarchoidea4, a clade that exhibits gigantism, we test the hypothesis that there was a decreased reliance on flight5,6,7 and find evidence for reduced selection on flight efficiency in this clade.”

Odd that these authors do not include the many examples of flightless pterosaurs, including derived and sometimes giant members of the Azhdarchidae.  They only say ‘there was a decreased reliance on flight.’

“Our approach offers a blueprint to objectively study functional and energetic changes through geological time at a more nuanced level than has previously been possible.”

There is no ‘blueprint’ here, only more misdirection and mythology. Sad that the works of professor Mike Benton have now become suspect following the present continuation of his long-standing pattern of cherry-picking and taxon exclusion favoring the textbooks and lectures that provide his income.

Andres B, Clark J and Xu, X 2014. The earliest pterodactyloid and the origin of the group. Current Biology 24:1011–1016 (2014).
Peters D 2000a. Description and Interpretation of Interphalangeal Lines in Tetrapods.  Ichnos 7:11-41.
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 2002. A New Model for the Evolution of the Pterosaur Wing – with a twist. Hist Bio 15: 277–301.
Peters D 2009. A reinterpretation of pteroid articulation in pterosaurs. Journal of Vertebrate Paleontology 29: 1327-1330
Venditti C, Baker J, Benton MJ, Meade A and Humphries S 2020. 150 million years of sustained increase in pterosaur flight efficiency. Nature https://doi.org/10.1038/s41586-020-2858-8

From the Nature comments section:
“The ancestors of pterosaurs were recovered twenty years ago (in Peters 2000) by simply adding Langobardisaurus, Cosesaurus, Sharovipteryx and Longisquama to four previously published analyses. Peters (2007) nested these bipedal taxa within the Lepidosauria by once again simply adding taxa. Omitting citations and omitting taxa results in statements like the following found in the Venditti et al. 2020 abstract: “in the absence of proto-pterosaur fossils, it is difficult to study how flight first evolved in this group.” Had the authors included Cosesaurus they would have known this taxon was flapping without flying due to a locked down, stem-shaped coracoid otherwise found only in birds and pterosaurs. Bats flap anchored by an analogous clavicle.”


Mid-sized Changyuraptor nests between big Ornitholestes and small Microraptor in the LRT

Han et al. 2014 brought us a new feathered theropod,
Changyuraptor yangi (Aptian, Early Cretaceous, HG B016). In the large reptile tree (LRT, 1720+ taxa) Changyuraptor nests between a bigger Ornitholestes and a smaller Microraptor… in that order (from big to medium to small).

By contrast
Han et al. nested Changyuraptor in unresolved nodes with Microraptor and others (see below), all close to dromaeosaurids and several nodes apart from Ornitholestes.

Figure 1. Changyuraptor reconstructed.

Figure 1. Changyuraptor reconstructed.

Changyuraptor is not so much a giant microraptorine
as a small ornitholestid. At least that’s the phylogenetic order.

Stem-like locked-down coracoids (= narrower, not taller) are traits that indicate flapping in Changyuraptor. Maybe it was a little too big to fly. That would have to wait for Microraptor and Sinornithosaurus. Even so, that extra thrust might have added speed to running. The display function would have given it a good bluff or a seductive show.

Figure 1. Changyuraptor to scale with Ornitholestes, Scriurumimus and Microraptor.

Figure 2. Changyuraptor to scale with Ornitholestes, Scriurumimus and Microraptor.

From the abstract:
“Microraptorines are a group of predatory dromaeosaurid theropod dinosaurs with aerodynamic capacity.”

By contrast the LRT nests microraptorines as bird mimics, closer to Ornitholestes than to dromaeosaurids and troodontids. Elongate coracoids were overlooked by Han et al. So this clade was flapping long flight feathers symmetrically, as birds, pterosaurs and bats do, not just carrying them around for show.

“These close relatives of birds are essential for testing hypotheses explaining the origin and early evolution of avian flight.”

By contrast, in the LRT microraptors are phylogenetically bird mimics, unrelated to the avian lineage.

“Here we describe a new ‘four-winged’ microraptorine, Changyuraptor yangi, from the Early Cretaceous Jehol Biota of China. With tail feathers that are nearly 30 cm long, roughly 30% the length of the skeleton, the new fossil possesses the longest known feathers for any non-avian dinosaur. Furthermore, it is the largest theropod with long, pennaceous feathers attached to the lower hind limbs (that is, ‘hindwings’).”

In the LRT Changyuraptor is transitional both in size and morphology between Ornitholestes and microraptorines. Earlier, without Changyuraptor, Ornitholestes and microraptorines nested together in the LRT.

“The lengthy feathered tail of the new fossil provides insight into the flight performance of microraptorines and how they may have maintained aerial competency at larger body sizes. We demonstrate how the low-aspect-ratio tail of the new fossil would have acted as a pitch control structure reducing descent speed and thus playing a key role in landing.”

On this topic, the coracoids of Changyuraptor and microraptorines are relatively small (smaller than in the chicken, Gallus) and Changyuraptor is relatively large. Plus Han et al. also overlooked the large sternum on Changyuraptor, but it lacks a ventral keel (distinct from Gallus). These traits indicate relatively small pectoral muscles, just barely suitable for weak flapping, but inadequate for flight on this mid-sized theropod. So Changyuraptor would have been a runner, not a flyer. Thus the feathered tail would not have needed pitch control if it stayed on ‘the runway.’ Perhaps, along with raised feathered elbows, raised tail feathers might have served as secondary sexual traits or bluffs designed to increased apparent size to marauding predators.

Diagnosis. A microraptorine dromaeosaurid theropod characterized by having the unique combination of traits: furcula more robust than that of Sinornithosaurus millenii and much larger than that of Tianyuraptor ostromi;

The LRT nests Tianyuraptor basal to tyrannosaurids along with Zhenyuanlong. Clavicles are separate and small elements in Ornitholestes, so the larger clavicles in Changyuraptor support the elongate coracoids.

“forelimb proportionally much longer when compared with hindlimb than in other microraptorines;

Figure 2. Changyuraptor limbs to scale.

Figure 3. Changyuraptor limbs to scale. Distinct from sister taxa, this taxon has a long forelimb.

True. Both Ornitholestes and Microraptor have relatively shorter fore limbs relative to the hind limbs.

“humerus much longer (>20% longer) than ulna as opposed to Microraptor zhaoianus, in which these bones are more comparable in length;”

The humerus of Changyuraptor is not >1.2x the ulna (Fig. 3), but the humerus of Ornitholestes (Fig. 4) is in that ratio range.

“metacarpal I proportionally shorter than in Sinornithosaurus millenii (1/4–1/5 versus 1/3);”

Metacarpal 1 is also shorter in Ornitholestes (Figs. 4, 5).

FIgure 6. Ornitholestes nests as a sister to Sciurumimus, between Compsognathus and Microraptor.

Figure 4. Ornitholestes nests as a sister to Sciurumimus, between Compsognathus and Microraptor.

Large, procumbent teeth
on a short skull can be seen even in ventral view on Changyuraptor.

Figure 3. Ornitholestes with a short metacarpal 1.

Figure 5. Ornitholestes with a short metacarpal 1.

“well-developed semi-lunate carpal covering all of proximal ends of metacarpals I and II as opposed to the small semi-lunate carpal that covers about half of the base of metacarpals I and II in most other microraptorines;”

Not illustrated in Ornitholestes.

“manual ungual phalanx of digit II is the largest, followed by that of digits I andt III, as opposed to Graciliraptor lujiatunensis in which the ungual of manual digit I is very small, and Sinornithosaurus millenii and Microraptor zhaoianus in which the unguals of manual digits I and II are comparable in size;”

See Ornitholestes (Figs. 4, 5) for available comparisons.

“ischium shorter than in Microraptor zhaoianus;

Ischium length is difficult to assess due to overlying elements.

“midshaft of metatarsal IV significantly broader than that of metatarsal III or metatarsal II, as opposed to G. lujiatunensis in which metatarsal IV is the narrowest;”

Comparables are difficult to assess in Ornitholestes due to lost metatarsals.

“mid-caudals roughly twice the length of dorsals as in Sinornithosaurus millenii as opposed to long caudal vertebrae in Microraptor zhaoianus;”

In Changyuraptor the midcaudals are 1.5x the dorsals length, and Sinornithosaurus is comparable. Note that Ornitholestes has a similarly hyper elongate tail.

“fewer caudal vertebrae (22 vertebrae) than Microraptor zhaoianus (25–26 vertebrae) and Tianyuraptor ostromi (28 vertebrae);”

Ornitholestes has many more than 20 caudal vertebrae.

“rectories significantly longer than in other microraptorines.”

Rectories not preserved in Ornitholestes.

This clade of microraptorine bird mimics evolved
by phylogenetic miniaturization. The coracoids became elongate (= narrower, not taller) and locked down for minimal flapping, much less than in extant fowl.

Han G, Chiapped LM, Ji S-A, Habib M, Turner AH, Chinsamy A, Liu X and Han L 2014. A new raptorial dinosaur with exceptionally long feathering provides insights into dromaeosaurid flight performance. Nature Communications DOI: 10.1038/ncomms5382



Fatal flaw in Taylori et al. 2019 hypothesis on avian flapping genesis

Taylori et al. 2019 report,
“From a mechanical standpoint, the forced vibrations excited by hindlimb locomotion stimulate the movement of wings, creating a flapping-like motion in response. This shows that the origin of the avian flight stroke should lie in a completely natural process of active locomotion on the ground.” We looked at this so-called ‘solution’ earlier here prior to peer-review.

The problems are:

  1. Caudipteryx is an oviraptorasaur, not in the line of bird origin.
  2. Caudipteryx has round, alternately sliding coracoids (like most tetrapods)
  3. Only elongate, immobile coracoids enable simultaneous wing flapping.
  4. Tiny Archaeopteryx is the basalmost bird that has elongate, immobile coracoids.
  5. Archaeopteryx is also the last common ancestor of all flapping birds, including members of the Enantiornithes

Phylogenetic analysis must precede all other biological testing.
Otherwise, like Taylori et al. you’re wasting your time imagining the genesis of flapping in a non-flapping taxon.

Talori YS, Zhao J-S, Liu Y-F, Lu W-X, Li ZH, O’Connor JK 2019. Identification of avian
flapping motion from non-volant winged dinosaurs based on modal effective mass analysis. PLoS Comput Biol 15(5): e1006846. https://doi.org/10.1371/journal.pcbi.1006846


UV light vs. LCA (last common ancestor) approach to flapping flight in birds

Schwarz et al. 2019
employed ultraviolet (UV) light to report, “In contrast to previous studies, we show that most of the vertebral column of the Berlin Archaeopteryx possesses intraosseous pneumaticity, and that pneumatic structures also extend beyond the anterior thoracic vertebrae in other specimens of Archaeopteryx. With a minimum Pneumaticity Index (PI) of 0.39, Archaeopteryx had a much more lightweight skeleton than has been previously reported, comprising an air sac-driven respiratory system with the potential for a bird-like, high-performance metabolism.

“The neural spines of the 16th to 22nd presacral vertebrae in the Berlin Archaeopteryx are bridged by interspinal ossifications, and form a rigid notarium-like structure similar to the condition seen in modern birds. this reinforced vertebral column, combined with the extensive development of air sacs, suggests that Archaeopteryx was capable of flapping its wings for cursorial and/or aerial locomotion.”

Schwarz et al. did not perform a phylogenetic analysis
nor did they mention anything about the elongate locked down coracoid present on this specimen. In the large reptile tree (LRT, 1445 taxa, subset Fig. 1) the Berlin specimen of Archaeopteryx (MB.Av.101) nests at the base of all flapping birds, including the Enantiornithes, the first clade to split off. As in the amniotic egg issue, the last common ancestor is where you find the genesis of traits common to all descendant taxa. So, Schwarz et al. are correct: the Berlin specimen is indeed close to the origin of flapping flight.

Figure 3. Subset of the LRT focusing on basal birds and pre-bird theropods. Note many of the various Solnhofen birds nest apart from one another and the Daiting specimen nests outside the birds (Aves).

Figure 1. Subset of the LRT focusing on basal birds and pre-bird theropods. Note many of the various Solnhofen birds nest apart from one another and the Daiting specimen nests outside the birds (Aves). The Berlin Archaoepteryx is the last common ancestor of all flapping birds.

It’s not the reinforced vertebral column
that determines if a bird (or pterosaur) flaps or not. It’s the elongation of an immobile coracoid these two flapping clades share in common at the genesis of this behavior.

Distinctlively different
due to lacking a coracoid, bats employ the hyper-elongation of the clavicle to do the same thing by convergence.

Figure 1. Generic freehand Archaeopteryx (Berlin specimen) from Schwarz et al. 2019, retraced from Wellnhofer 2008 compared to bone-by-bone tracing for ReptileEvolution.com.

Figure 2. Generic freehand Archaeopteryx (Berlin specimen) from Schwarz et al. 2019, retraced from Wellnhofer 2008 compared to bone-by-bone tracing for ReptileEvolution.com. Wellnhofer’s drawing appears to be a generic Archaeopteryx. Tracings of all specimens show no two are alike.

One more thing…
if possible, don’t freehand your reconstructions (Fig. 2) and don’t redraw freehand reconstructions from Wellnhofer 2008 ~ especially if you’re going to go through all the trouble of extracting more precise data on a fossil than has been recovered before. Do your own more precise bone tracings and reconstructions!

Schwarz D, Kundrat M, Tischlinger H, Dyke G and Carney RM 2019. Ultraviolet light illuminates the avian nature of the Berlin Archaeopteryx skeleton. Nature.com
Wellnhofer P 2008. Archaeopteryx. Der Urvogel von Solnhofen. (Verlag Dr. Friedrich Pfeil, München), pp. 256.

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

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

SVP 2018: Stages in the origin of avian flight

Hartman, Mortimer and Lovelace 2018
reconstruct the origin of avian flight in a series of stages:

  1. Acquisition of theropod characters unrelated to avian flight, including bipedalism, three fingered hands, a furcula, and filamentous epidermal structures.
  2. Acquisition of characters directly exapted for flight such as enlarged forelimbs, pennaceous feathers on the forelimbs and tail, increased angle between scapula and distal coracoid, and laterally facing glenoid fossae.
  3. Characters acquired due to aerial locomotion, including tertial feathers, expansion of the flight stroke and associated muscles, and in more derived taxa an alula and reduction of the distal caudal series to a pygostyle.
  4. Characters associated with higher endurance crown avian-style flight including enlarged keeled sterna, hinged sternal ribs, loss of gastralia, and well-developed caudal air sacs.
Figure 1. Xiaotingia, the proximal outgroup to the Thermopolis specimen of Solnhofen birds, the basalmost bird.

Figure 1. Xiaotingia, the proximal outgroup to the Thermopolis specimen of Solnhofen birds, the basalmost bird.

Based on the outgroup taxon, Xiaotingia
(Fig. 1) and the basalmost Solnhofen bird, the Thermopolis specimen, missing from the above list of traits are:

  1. phylogenetic miniaturization
  2. more gracile bones overall
  3. a smaller skull
  4. a more gracile neck
  5. a longer tail
  6. an elongate coronoid, which signals the start of flapping
  7. a larger olecranon process
  8. avian-style wrist
  9. a more robust retro pedal digit 1 with a larger ungual

Hartman, Mortimer and Lovelace conclude:
“Stage 2 taxa with small body size and enlarged forelimbs may have utilized wing assisted incline running (WAIR) to access trees despite lacking unambiguously arboreal characters, breaking the ground-up/trees-down dichotomy.” Yes, but this seems like old news as Ken Dial published the same conclusion in 2003. Where in the author’s list is the elongate coracoid common to all flapping tetrapods? …and found in non-avian convergent micro raptors and sinornithosaurs?

…and the authors continue:
“Several Stage 2 taxa independently approached Stage 3 conditions, including some
microraptorians, Rahonavis, Archaeopteryx and scansoriopterygids; this suggests that
WAIR enabled several parallel experiments with aerial locomotion.” Good points first noted in the LRT, except that scansoriopterygids are birds when more Solnhofen birds are added to the taxon list. (Need to consider all Solnhofen birds as taxa, not just have one and label it Archaeopteryx). T-rex ancestor, Zhenyuanlong might also be added to this list, given its large wing feathers.

Dial KP 2003. Wing-assisted incline running and the evolution of flight.  Science 299:402-404.
Hartman S, Mortimer M and Lovelace DM 2018. A testable macroevolutionary framework for character acquisition in the origin of avian flight. SVP abstracts.

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

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.

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 x. Calcaneal spur in Zhangheotherium. Not venomous, but perhaps to anchor a uropatagium.

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

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 x. Zhangheotherium showing possible extradermal membranes (green) with keratinous scales (red) and several newborns scattered in the abdominal area, similar to Monodelphis in figure x.

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 1. 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.

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 1. Wondering if Chriacus had an inverted stance and dermopteran membranes? Comparisons to Onychonycteris and Pteropus.

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.

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

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.

Axial rotation: fingers in pterosaurs, toes in birds

A somewhat recent paper by Botelho et al. 2015
looked at the embryological changes that axially rotate metatarsal 1 to produce a backward-pointing, opposable, perching pedal digit 1 (= hallux).

Hallux rotation phylogenetically
Botelho reports: Mesozoic birds closer than Archaeopteryx to modern birds include early short-tailed forms such as the Confuciusornithidae and the toothed Enantiornithes. They present a Mt1 in which the proximal portion is visibly non-twisted, while the distal end is offset (“bent”) producing a unique “j-shaped” morphology. This morphology is arguably an evolutionary intermediate between the straight Mt1 of dinosaurs and the twisted Mt1 of modern birds, and conceivably allowed greater retroversion of Mt1 than Archaeopteryx.”

“D1 in the avian embryo is initially not retroverted9, and therefore becomes opposable during ontogeny, but no embryological descriptions address the shape of Mt1, and no information is available on the mechanisms of retroversion.”

Figure 1. Pes of the most primitive Archaeopteryx, the Thermopolis specimen.

Figure 1. Pes of the most primitive Solnhofen bird, the Thermopolis specimen. This digit 1 never left the substrate.

In Tyrannosaurus,
(Fig. 2) the entire metatarsal 1 with pedal digit 1 is rotated just aft of medial by convergence. It’s not axially rotated. It’s just attached to the palmar side of the pes. This pedal digit 1 was elevated above the substrate.

Figure 2. The semi-retroverted pedal digit 1 of Tyrannosaurus rex in two views.

Figure 2. The semi-retroverted pedal digit 1 of Tyrannosaurus rex in two views. This digit 1 was elevated above the substrate.

In some birds
like the woodpecker, Melanerpes, and the unrelated roadrunner, Geococcyx, pedal digit 4 is also retroverted. Sorry, I digress.

Further digression
The axial rotation of pedal digit 1 in birds is convergent with the axial rotation of metacarpal 4 in Longisquama (Fig. 3) and pterosaurs. In both taxa the manus was elevated off the substrate and permitted to develop in new ways. Manual digit 4 never leaves an impression in pterosaur manus tracks… because it is folded, like a bird wing, against metacarpal 4. In Longisquama such extreme flexion is not yet possible.

Figure 1. Longisquama left and right manus traced using DGS then reconstructed (below). This is a very large hand for a fenestrasaur and manual digit 4 is oversized, as in pterosaurs.

Figure 3. Longisquama left and right manus traced using DGS then reconstructed (below). This is a very large hand for a fenestrasaur and manual digit 4 is oversized and the metacarpal is axially rotated, as in pterosaurs. Manual digit 5 is useless, but not yet a vestige. A pteroid is present, as in Cosesaurus. The coracoid is elongate as in birds. The sternum, interclavicle and clavicle are assembled into a single bone, the sternal complex, as in pterosaurs.

Note the lack of space between
the radius and ulna in Longisquama. This is what also happens in pterosaurs. It prevents the wrist from pronating or supinating, as in birds and bats… which means, the forelimb is flapping, not pressing against the substrate, nor grasping prey. That means all those images of Longsiquama on all fours are bogus. Now you know.

So now we come full circle
While the toes of birds axially rotate and the wing metacarpal of pterosaurs axially rotates, the forearms of birds, pterosaurs and Longisquama do not axially rotate. No one wants their wing to twist.

Botelho JF, Smith-Paredes D, Soto-Acuña S, Mpodozis J, Palma V and Vargas AO 2015. Skeletal plasticity in response to embryonic muscular activity underlies the development and evolution of the perching digit of birds. Article in http://www.Nature.com/Scientific Reports · May 2015 DOI: 10.1038/srep09840

Flapping before flight

This is a long overdue and very welcome paper
Many paleontologists of the past thought flight appeared after gliding. This is the so-called trees down theory seen in this PBS video on Microraptor. Others thought the flight stroke appeared while clutching bugs in the air. This is the so-called ground up theory. Through experimentation Ken Dial found out that baby birds armed with only protowings flapped them vigorously to help them climb trees, no matter the angle of incline. Now the kinematics of this wing/leg cooperation are presented in Heers et al. 2016, students of Ken Dial.

Key thoughts from the abstract:
“Juvenile birds, like the first winged dinosaurs, lack many hallmarks of advanced flight capacity. Instead of large wings they have small “protowings”, and instead of robust, interlocking forelimb skeletons their limbs are more gracile and their joints less constrained. Such traits are often thought to preclude extinct theropods from powered flight, yet young birds with similarly rudimentary anatomies flap-run up slopes and even briefly fly, thereby challenging longstanding ideas on skeletal and feather function in the theropod-avian lineage.
For the first time, we use X-ray Reconstruction of Moving Morphology to visualize skeletal movement in developing birds. Our findings reveal that developing chukars (Alectoris chukar) with rudimentary flight apparatuses acquire an “avian” flight stroke early in ontogeny, initially by using their wings and legs cooperatively and, as they acquire flight capacity, counteracting ontogenetic increases in aerodynamic output with greater skeletal channelization.Juvenile birds thereby demonstrate that the initial function of developing wings is to enhance leg performance, and that aerodynamically active, flapping wings might better be viewed as adaptations or exaptations for enhancing leg performance.”
Figure 2. Cosesaurus running and flapping - slow.

Figure 1. Cosesaurus running and flapping – slow.

The same theory
can be applied to the development of wings in fenestrasaurs (Fig. 1) evolving into pterosaurs (Fig 2), as shown several years ago, but does not play a part in the development of flapping wings in bats, which do not walk upright and bipedally.
Quetzalcoatlus running like a lizard prior to takeoff.

Figure 2 Quetzalcoatlus running like a lizard prior to takeoff. Click to animate.

It should be obvious
that competing take-off theories for pterosaurs (Fig. 3) do not take into account this theory on the origin of flapping. Just one more reason not to support the forelimb wing launch hypothesis that has become so popular with ptero-artists recently.

Unsuccessul Pteranodon wing launch based on Habib (2008).

Figure 3. Unsuccessul Pteranodon wing launch based on Habib (2008) in which the initial propulsion was not enough to permit wing unfolding and the first downstroke.

getting into the air is difficult if you’ve never done it before. Using both your arms AND your legs to get up speed is a good idea that has worked in the past and in present day laboratories.

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