Some time during the last several hours (while I was asleep), Tet Zoo reached the three million hits mark. Yes, three million hits in two years (Tet Zoo ver 2 was launched on Jan 31st 2007). A noble achievement, I'm sure you'll agree. Due to workload and assorted other commitments, I still don't have anything major new to post (how the hell do the more prolific bloggers do it?), though there was the new salamander thing yesterday - knocked up very quickly on the spur of the moment - and I've also just produced a new SV-POW! article. Inspired by a comment Nathan Myers left here recently about the bat diphyly issue, I've decided to re-post an old article from ver 1. As with other re-posted pieces, I expect it to be new to some or even most readers given that it was published in 2006. Important: please note that I have not (post-2006) substantially updated or modified the article so, by definition, it is out of date and primarily of historical interest (I did, however, just add some new text on microbat diphyly, as the old text was a bit misleading.. and I added a new bit on Eocene bats as well). However, it serves as useful background reading and generated a lot of interest last time it appeared...

Mention 'flying primate' and most zoologists will think you're referring to the well known, controversial proposal of John Pettigrew of the University of Queensland. Initially basing his conclusions on retinotectal organization (viz, the way in which data from the retina is processed in the brain), Pettigrew (1986) argued that megabats (the group that includes fruit bats like the one shown above) are not close relatives of microbats (the mostly small, mostly insectivorous bats that mostly use echolocation), but that they're actually flying primates, of a sort (read on). If this is right, then Chiroptera [the proper name for the bats] is not monophyletic, and true flight evolved at least twice among mammals. Furthermore, primates and their close relatives are more diverse than conventionally thought, and include an impressive radiation of hitherto misclassified volant species.

In more detailed papers, Pettigrew (1991) and Pettigrew et al. (1989) marshaled evidence from eye, brain and spinal cord anatomy, fore- and hindlimb, finger and metacarpal proportions, and haemoglobin sequences, and again concluded that megabats and primates shared a common ancestor. Microbats, they argued, were not close relatives of megabats and must have affinities elsewhere. Pettigrew et al. (1989) further argued that colugos (aka flying lemurs, or dermopterans) were also part of the megabat-primate clade, and are essentially late-surviving relics which resembled the common ancestor of this group [Sunda flying lemur Galeopterus variegatus (traditionally Cynocephalus variegatus) shown below, from wikipedia. I've rotated the image so that the weirdness of the animal is more obvious].

Pettigrew and colleagues weren't the first to question bat monophyly: John E. Hill of the then British Museum (Natural History) had done this as early as 1976, Smith & Madkour (1980) argued that micro- and megabats were of separate origins, and Hill & Smith (1984), in one of the best and oft-cited overviews of bat evolution and biology, expressed scepticism of bat monophyly and a preference for megabat-primate affinities (p. 36).

The 'flying primate' theory [or hypothesis]... success and failure

Popularly, Pettigrew et al.'s notion that megabats are closer to primates than to microbats became characterized as the 'flying primate' theory, and Pettigrew et al. used this term in their papers. This characterization isn't accurate, however, as Pettigrew et al. (1989) specifically stated that, within their favoured phylogenetic scheme, megabats would be outside of the clade Primates, and thus not primates in the true sense (p. 551).

I must admit that the 'flying primate' theory has a great deal of intuitive appeal, and this probably explains why it's become both well known and much written about. Colin Tudge wrote about it in The Independent (a British broadsheet newspaper) for example (his article was titled 'That's no bat, that's my brother'), and it isn't every day that problem areas within the higher-level phylogenetics of placental mammals make it into daily newspapers. Why is the 'flying primate' hypothesis intuitively appealing? Perhaps because it appears to have reasonable and easily understood character support and is exciting in contending that a complex and strongly modified bit of morphology - namely the bat wing, with its bizarre elongated fingers and patagial membranes - evolved independently more than once. The fact that it has implications for our own origins might add to its popular appeal (read on).

The accompanying image by Peter Schouten, commissioned by John Pettigrew, depicts the 'flying primate' hypothesis in graphic form: note that colugos and megabats branch off from the primate lineage, and aren't alongside microbats. This image is borrowed from Pettigrew's Neuroscience UQ site.

However, from the start most bat experts had a problem with the concept: Wible & Novacek (1988) showed how numerous skeletal and soft tissue features 'strongly support the inclusion of megabats and microchiropterans within the single order Chiroptera' (p. 1). Simmons et al. (1991) argued that Pettigrew's entire approach to the bat monophyly question was flawed (in that it seemed based on the assumption that one bit of data - like retinotectal organization - could outweigh all the rest), Thewissen & Babcock (1992) argued that the detailed anatomy of wing musculature best supported bat monophyly, while Bailey et al. (1992) and Ammermann & Hillis (1992) found that genetic data better supported the case for bat monophyly than that for diphyly. Bailey et al.'s paper was even titled 'Rejection of the 'flying primate' hypothesis', and in an accompanying news piece in Science Ann Gibbons wrote how the 'flying primate' hypothesis was 'heading for a crash landing'. A comprehensive overview of all the data supporting bat monophyly was provided by Nancy Simmons (1994).

Horseshoe bats and kin group with megabats

DNA-based studies later published by Pettigrew and his colleagues produced a new, even more surprising result: rhinolophoids (the horseshoe bats and their relatives) were consistently found to group together with megabats, the implication now being that Microchiroptera might be non-monophyletic* (Hutcheon et al. 1998, Kirsch & Pettigrew 1998, Pettigrew & Kirsch 1998). The existence of a rhinolophoid-megabat clade has also been supported by other research teams (e.g., Teeling et al. 2000, 2002, Liu et al. 2001) but note that many of these studies (Hutcheon et al. 1998, Teeling et al. 2000, 2002, Liu et al. 2001) did not support Pettigrew's idea of chiropteran diphyly [cladogram below, from Hutcheon et al. (1998), shows megabats forming a clade with rhinolophoids. Hutcheon & Kirsch (2006) proposed that the names Pteropodiformes and Vespertilioniformes should be used for the two major clades of crown-group bats].

* I struggle to appreciate in this case whether the group is non-monophyletic or merely paraphyletic. After all, Microchiroptera is still there: it just turns out that a supposedly distinct group (Megachiroptera) is nested within it. Help me out.

Let's suppose for a moment however that Pettigrew and colleagues are right, and that neither Chiroptera nor Microchiroptera are monophyletic. Suppose also that bats are members of the placental mammal group Archonta - an idea that was quite widely accepted until recently (read on). Archonta was first named by William King Gregory in 1910* to house Scandentia (tree shrews), Chiroptera, Dermoptera and Primates (Gregory also included sengis/elephant shrews within Archonta, but they were later removed from it as their affinities clearly lie elsewhere). As the only mammalian clade whose constituent groups are all tied to a climbing lifestyle, it was always very nice to have the bats in there, given that an arboreal origin for bat flight has always been favoured by everyone who's ever pondered the issue.

* It's always been problematical that archontan monophyly has only ever been supported by two morphological characters: the anatomy of the penis, and the shape of one of the facets on the astragalus. By their genitals and ankles ye shall know them. If you're wondering, Archonta means 'ruling beings'. Yuck.

As you see from the little cladogram I've knocked up here, bat diphyly and archontan monophyly makes it at least possible - and phylogenetically parsimonious - that flight was primitive for the megabat-primate clade, or in other words that primates are secondarily flightless. That's right: you and me, and other apes, and lemurs, tarsiers and monkeys all descend from flying, winged proto-primates. If I were George Olshevsky I might dub this the 'Bats Come First' model [now you know what I'm talking about: see The 'Birds Come First' hypothesis of dinosaur evolution and Birds Come First - oh no they don't!]

But, no, it wasn't to be. Bat diphyly is not currently favoured by the evidence, and even Archonta has now fallen by the wayside: DNA-based phylogenies now indicate that, while Scandentia, Dermoptera and Primates probably do form a clade - the newly dubbed Euarchonta - bats aren't close relatives of euarchontans at all. Instead they go elsewhere within the placental mammal clade Laurasiatheria, being (most surprisingly) closest to carnivorans, perissodactyls and artiodactyls (e.g., Murphy et al. 2001, Liu et al. 2001). And what of the idea that microbats aren't monophyletic? One recent review found that this arrangement was not as well supported by the data as is the traditional view of microbat monophyly (Jones et al. 2002): however, this was a supertree analysis and hence its results were heavily skewed by the fact that 'the majority of source topologies support microbat monophyly' (p. 223). Other morphological and molecular analyses have provided further support for the monophyly of a rhinolophoid + megabat clade that is nested within a monophyletic Chiroptera (e.g., Teeling et al. 2005, Hutcheon & Kirsch 2006, Simmons et al. 2008).

As always the full story that I wanted to cover is even more complex than what's related here. I haven't even mentioned the paromomyids: a group of Eocene euarchontans proposed at one time to be colugo-like gliders and thus implicated in the issue of primate and colugo origins. Nor have I discussed the little nyctitheres, a poorly known and long-mysterious Eocene-Oligocene group that appear to have been primitive, scansorial relatives of euarchontans. In fact comparison of nyctitheres with bats and euarchontans led Hooker (2001) to restate the case for archontan monophyly, with Deccanolestes from the Late Cretaceous of India being the oldest member of the group according to his study. Genetic data clearly doesn't favour archontan monophyly right now, but there is still at least some morphological support for it. A common problem (and, since this article was written, we have a new, particularly primitive bat: Onychonycteris finneyi from the late early Eocene of Wyoming (Simmons et al. 2008). Shown here, acting as covergirl/boy (from wikipedia). It now seems that Onychonycteris and other early bats (Icaronycteris, Archaeonycteris, Hassianycteris and Palaeochiropteryx) are basal to a chiropteran crown-group that includes all extant forms including megabats).

Update (added 5-8-2006): a new paper just published by Nishahara et al. (2006) has reported new genetic support for a laurasiatherian clade composed of bats, perissodactyls, carnivorans and pangolins. They name this clade Pegasoferae, a name derived by uniting Pegasus (in their view a sort of bat-perissodactyl combination) with Ferae (the name they use for the carnivoran + pangolin clade).

For previous Tet Zoo articles on bats see...

Refs - -

Ammerman, L., & Hillis, D. (1992). A Molecular Test of Bat Relationships: Monophyly or Diphyly? Systematic Biology, 41 (2), 222-232 DOI: 10.1093/sysbio/41.2.222.

Bailey, W. J., Slightorn, J. L. & Goodman, M. 1992. Rejection of the 'flying primate' hypothesis by phylogenetic evidence from the globin gene. Science 256, 86-89.

Hill, J. E. & Smith, J. D. 1984. Bats: a Natural History. British Museum (Natural History), London.

Hooker, J. J. 2001. Tarsals of the extinct insectivoran family Nyctitheriidae (Mammalia): evidence for archontan relationships. Zoological Journal of the Linnean Society 132, 501-529.

Hutcheon, J. M. & Kirsch, J. A. W. 2006. A moveable face: deconstructing the Microchiroptera and a new classification of extant bats. Acta Chiropterologica 8, 1-10.

- ., Kirsch, J. A. W. & Pettigrew, J. D. 1998. Base-compositional biases and the bat problem. III. The question of microchiropteran monophyly. Philosophical Transactions of the Royal Society of London B 353, 607-617.

Jones, K. E., Purvis, A., MacLarnon, A., Bininda-Emonds, O. R. P. & Simmons, N. B. 2002. A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biological Reviews 77, 223-259.

Kirsch, J. A. W. & Pettigrew, J. D. 1998. Base-compositional biases and the bat problem. II. DNA-hybridization trees based on AT- and GC-enriched tracers. Philosophical Transactions of the Royal Society of London B 353, 381-388.

Liu, F.-G. R., Miyamoto, M. M., Freire, N. P., Ong, P. Q., Tennant, M. R., Young, T. S. & Gugel, K. F. 2001. Molecular and morphological supertrees for eutherian (placental) mammals. Science 291, 1786-1789.

Murphy, W. J., Eizirik, E., Johnson, W. E., Zhang, Y. P., Ryder, O. A. & O'Brien, S. J. 2001. Molecular phylogenetics and the origins of placental mammals. Nature 409, 614-618.

Nishihara, H., Hasegawa, M. & Okada, N. 2006. Pegasoferae, an unexpected mammalian clade revealed by tracking ancient retroposon insertions. Proceedings of the National Academy of Sciences 103, 9929-9934.

Pettigrew, J. D. 1986. Flying primates? Megabats have the advanced pathway from eye to mid-brain. Science 231, 1304-1306.

- . 1991. Wings or brains? Convergent evolution in the origin of bats. Systematic Zoology 40, 199-216.

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- ., Jamieson, B. G. M., Robson, S. K., Hall, L. S., McAnally, K. I. & Cooper, H. M. 1989. Phylogenetic relations between microbats, megabats and primates (Mammalia: Chiroptera and Primates). Philosophical Transactions of the Royal Society of London B 325, 489-559.

Simmons, N. B. 1994. The case for chiropteran monophyly. American Museum Novitates 3103, 1-54.

- ., Novacek, M. J. & Baker, R. J. 1991. Approaches, methods, and the future of the chiropteran monophyly controversy: a reply to J. D. Pettigrew. Systematic Zoology 40, 239-243.

- ., Seymour, K. L., Habersetzer, J. & Gunnell, G. F. 2008. Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451, 818-821.

Smith, J. D. & Madkour, G. 1980. Penial morphology and the question of chiropteran monophyly. In Wilson, D. E. & Gardner, A. L. (eds) Proceedings of the 5th International Bat Research Conference. Texas Tech Press (Lubbock), pp. 347-365.

Teeling, E. C., Madsen, O., Van Den Bussche, R. A., de Jong, W. W., Stanhope, M. J. & Springer, M. S. 2002. Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats. Proceedings of the National Academy of Sciences 99, 1431-1436.

- ., Scally, M., Kao, D. J., Romagnoll, M. L., Springer, M. S. & Stanhope, M. J. 2000. Molecular evidence regarding the origin of echolocation and flight in bats. Nature 403, 188-192.

Teeling, E. C., Springer, M. S., Madsen, O., Bates, P., O'Brien, S. J., Murphy, W. J. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science, 307, 580-584.

Thewissen, J. G. M. & Babcock, S. K. 1992. The origin of flight in bats. BioScience 42 (5), 340-345.

Wible, J. R. & Novacek, M. J. 1988. Cranial evidence for the monophyletic origin of bats. American Museum Novitates 2911, 1-19.