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Again, reading from outdated textbooks,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.

The basalmost primate in the LRT is alive and living in Madagascar!

Now you have a choice.
Either go out looking for crumbling bits and pieces of basal primate jaws and teeth over vast stretches of badlands… Or go to Madagascar to study basal primates in the wild, and have them feeding from your hand, according to the latest addition to the LRT.

The gray mouse lemur,
(Microcebus murinus; Figs. 1, 2) nests at the base of the all the tested primates in the large reptile tree (LRT, 1692+ taxa; subset Fig. 3), basal to both larger adapid lemurs, Notharctus and Smilodectes.

Figure 1. The gray mouse lemur (Microcebus murinus) nests basal to primates in the LRT.

Figure 1. The gray mouse lemur (Microcebus murinus) nests basal to primates in the LRT.

This largest species in this smallest genus of primates
also nests between two tree shrew taxa, Tupaia (basal to Glires) and Ptilocercus (Fig. 4; basal to Volitantia).

Though living today in Madagascar forests,
Microcebus likely radiated during the Cretaceous, prior to the splitting of Madagascar from Africa 88 mya. Later it gave rise to all extinct and extant adapids and lemurs on that island.

Millions of years ago lemurs were
worldwide in distribution. Now only a few lemurs find refuge in Madagacar. and only in Madagascar.

Figure 2. The skull of Microcebus murinus from Digimorph.org and used with permission. Here colors mark bones.

Figure 2. The skull of Microcebus murinus from Digimorph.org and used with permission. Here colors mark bones.

Microcebus murinus (Miller 1777) is the extant gray mouse lemur an omnivore found only in Madagascar. This nocturnal arboreal basalmost primate in the LRT forages alone, but sleeps in groups, sharing tree holes during the day. Twin babies are typical. Offspring can reproduce after one year. Lifespan extends to ten years. The eyes are large, typical of nocturnal mammals. Relatives include Hapalodectes and Ptilocercus. Descendants include Notharctus and Smilodectes.

The newly expanded clade Scandentia (tree shrews) now unites
Volitantia (bats + pangolins + colugos), Primates and Glires (rodents, rabbits, multituberculates and kin) in the LRT, subset Fig. 3). The addition of Microcebus as the smallest lemur held the possibility that it was the most basal form or one leading to smaller galagos and tarsiers. This time Microcebus turned out to be more primitive.

Figure 3. Subset of the LRT focusing on the clade Scandentia (tree shrews) and the three arboreal clades that arise from it.

Figure 3. Subset of the LRT focusing on the clade Scandentia (tree shrews) and the three arboreal clades that arise from it.

With the addition of Microcebus to the LRT,
the extant pen-tailed tree shrew, Ptilocercus (Fig. 4) nests basal to colugos, which also lack upper incisors. That means an older, more plesiomorphic fossil taxon with a complete set of upper incisors is out there waiting to be discovered somewhere in Early Jurassic fossil beds.

Figure 4. Ptilocercus is a sister to Microcebus nesting with colugos.

Figure 4. Ptilocercus is a sister to Microcebus nesting with colugos.

Paleontologists have been looking for the ancestor of primates,
colugos and bats for ages. They find fewer and smaller bony scraps the deeper they look.

Here’s a solution:
Add extant taxa. Phylogenetic analyses that includes extant taxa can sometimes help by nesting late survivors at basal nodes. Sure the fossil taxa are the real ancestors. Sure, living lemurs are late survivors, radiating into new morphologies and niches, but the soft, cuddly, active chatterboxes (Fig. 1) are still worth studying and scoring.


References
Miller JF 1777. Cimelia Physica p.25

wiki/Microcebus

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

Tweaking Palaechthon (basal Volitantia)

Kay and Cartmill 1977 wrote:
“The Middle Paleocene paromomyid Palaechthon nacimienti has the most primitive cranial anatomy known for any plesiadapoid. In relative size and functional morphology, its molars resemble those of primates and tree shrews known to feed largely on insects. Its orbits were small, laterally directed, and widely separated, and the relative size of its infraorbital foramen shows that it had well-developed facial vibrissae resembling those of extant erinaceids. Its anterior dentition was probably also hedgehog-like. These features suggest that it was a predominantly terrestrial insect-eater, guided largely by tactile, auditory and olfactory sensation in its pursuit of prey. Adaptations to living in trees and feeding on plants probably developed in parallel in more than one lineage descended from the ancestral plesiadapoids. A new genus and species of paromomyid, Talpohenach torrejonius, is erected for material originally identified as Palaechthon.”

This was done in the days before software phylogenetic analysis.
In the large reptile tree nests (LRT, 1413 taxa) Palaechthon as a sister to the dermopterans, like Cynocephalus, both derived from basal Carnivora, like Vulpavus (Fig. 1). All of these taxa are basal to Primates in the LRT.

Palaechthon is known from several partial specimens
combined to make the incomplete skull drawing shown here (Fig. 1).

Figure 1. Palaechthon compared to outgroup, Vulpavus, and sister, Cynocephalus using drawings from Kay and Cartmill 1974. Colors added.

Figure 1. Palaechthon compared to outgroup, Vulpavus, and sister, Cynocephalus using drawings from Kay and Cartmill 1974. Colors added.

Palaechthon nacimienti (Wilson and Szalay 1972) ~4cm skull length, middle Palaeocene, was originally and traditionally considered a basal plesiadapiform (traditionally considered a clade of basal primates). Here derived from a sister to the basal placental and carnivoran, Vulpavus, Palaechthon phylogenetically nests with Cynocephalus, the colugo. The premaxilla is missing and may have been nearly toothless, as in the colugo. Distinct from Vulpavus, but as in Cynocephalus, and the basalmost eutherian, Caluromys, four molars are present in Palaechthon.

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

Figure 2. Cynocephalus, the flying lemur, shares many traits with Ptilocercus and basal bats.

Phylogenetic bracketing
makes Palaechthon an arboreal taxon, possibly with a prehensile tail. Kay and Cartmill 1974 imagined large, rodent-like teeth emerging from the missing premaxilla and missing anterior dentary (Fig. 1). Phylogenetic bracketing indicates just the opposite—tiny anterior teeth, as shown in Vulpavus and Cynocephalus. The auditory bulla was probably small, as indicated by phylogenetic bracketing. The post-dentary part of the skull was probably short, as in Cynocephalus.

Figure 1. Ignacius and Plesiadapis nest basal to Daubentonia in the LRT.

Figure 3. Ignacius and Plesiadapis nest basal to Daubentonia in the LRT.

The present ‘tweaking’
benefits from more recent additions to the LRT that provided more clues to the closest relatives of Palaechthon, cementing relationships recovered years earlier. First hand access did not give Kay and Cartmill more insight into the relationships of Palaechthon, a basal member of the clade Volitantia.They presumed from the start that it was a primate ancestor, close to Plesiadapis. Both presumptions have been refuted by the LRT, which tests both basal primates and plesiadapiformes, now nesting within Glires. Based on the appearance of descendant taxa in the Middle Jurassic, Palaechthon had its genesis in the Early Jurassic.


References
Fleagle JG 1988. Primate Adaptation and Evolution. Academic Press: New York
Kaplan M 2012. Primates were always tree-dwellers. Nature. doi:10.1038/nature.2012.11423
Kay RF and Cartmill M 1974. Skull of Palaechthon nacimienti. Nature 252:37–38.
Kay RF and Cartmill M 1977. Cranial Morphology and Adaptation of Palaechthon nacimienti and Other Paromomyidae (Plesiadapoidea, Primates), with a Description of a New Genus and Species. Journal of Human Evolution, Vol. 6, 19-53.
Sloan RE and Van Valen L 1965. Cretaceous mammals from Montana. Science 148:220–227
Van Valen L and Sloan R 1965. The earliest primates. Science. 150(3697): 743–745.
Wible JR, Rougier GW, Novacek MJ and Asher RJ 2007. Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary.” Nature volume 447: 1003-1006
Wilson RW and Szalay FS 1972. American Museum Novitates 2499:1.