The vesper bat family tree: of myotines, plecotins, antrozoins, and all those cryptic species (vesper bats part II)

So, in the previous article we introduced vesper bats (sensu lato) as a whole, covered the idea that they're pretty diverse in morphology and behaviour, and also looked quickly at where they seem to fit within the bat family tree as a whole. As you'd predict for a diverse group of over 400 species, there have been numerous attempts to group these many species into clades, and to work out the patterns of evolution within the group. A large number of 'subfamilies' and 'tribes' have been named for different assemblages of vesper bat species, though a comparatively small number of useful characters - and a great difference of opinion as to which characters are most informative - has resulted in quite different classifications. You'll definitely want to skip this whole article if identifying clades and phylogenetic branching patterns bores you to tears [the adjacent cladogram is deliberately shown as annoyingly small - a larger version is below]. Right, off we go...

While no two classification systems have ever been exactly alike, Vespertilionidae has often been divided into Vespertilioninae, Miniopterinae (long-fingered bats or bent-winged bats), Murininae (tube-nosed bats) and Kerivoulinae (painted bats or woolly bats). In turn, Vespertilioninae has conventionally been split into seven tribes: Myotini (mouse-eared bats and kin), Plecotini (long-eared bats and kin), Vespertilionini (pipistrelles, serotines and so on), Nycticeini or Nycticeiini (broad-nosed bats and kin), Lasiurini (hoary bats), Antrozoini (pallid bats and kin) and Nyctophilini (Australasian big-eared bats) (e.g., Tate 1942, Simpson 1945, Koopman & Jones 1970, Hill & Harrison 1987, Koopman 1994, McKenna & Bell 1997). The 'key features' typically used to distinguish these groups (and classify individual species) are predominantly found in the dentition and mostly relate to the absence or presence of upper incisors and premolars (Tate 1942).

Volleth & Heller (1994) used chromosomal data to produce the first cladistic evaluation of vesper bats: they found miniopterines to be outside the clade that included all other lineages; kerivoulines, murinines and myotins to be 'basal' taxa; and plecotins and nycticeiins to be outside an (eptesicin + (vespertilionin + pipistrellin)) clade. A substantially simplified version of their cladogram is shown here...

A note on nomenclature: in keeping with some (but not all) previous authors, I'm going to use -in endings for the vernacular names of 'tribes' in order to help distinguish them from 'subfamilies'. So, members of Plecotini get referred to as plecotins, while members of Myotinae get referred to as myotines (though as myotins when authors have regarded them as 'tribe' Myotini, as above). Note that you may well need to keep up with the names of the various groups if you want the following discussion to make sense, sorry.

Since about 2000, various researchers have used DNA-based analyses to examine the relationships among vesper bat taxa, and many of the results have been at odds with the traditional, morphology-based relationships hypothesised by Tate (1942) and others. While competing conclusions such as these often used to be portrayed as a 'molecules vs morphology' issue, it's increasingly clear that both sources of data have their drawbacks; as Van Den Bussche & Hoofer (2004) said "much of the discrepancy among these studies is due to improper choice of out-group, limited taxonomic sampling, or both" (p. 321).

A major, comprehensive phylogenetic effort dedicated specifically to vesper bats was produced by Hoofer & Van Den Bussche (2003): they recovered Miniopterinae as the sister-group to all other vesper bats (more on that - and on what it means for the taxonomic status of bent-winged bats - later on). However, they found Murininae and Kerivoulinae to be sister-taxa. The mouse-eared bats (Myotis) seemed to be the sister-group to the Murininae + Kerivoulinae clade, and vespertilionines were the sister-group to this newly recovered clade. The huge Vespertilioninae included a major clade formed of three sub-clades that corresponded to Nycticeini or Nycticeiini (broad-nosed bats and kin), a pipistrelle-noctule clade that they termed Pipistrellini, and a clade of pipistrelle-like bats that they termed Vespertilionini. Outside this large clade, most other vespertilionines were in a polytomy: this included Scotophilini (house bats), Antrozoini (pallid bats and kin), the various genera usually included in Plecotini (long-eared bats and kin), Lasiurini (hoary bats), Perimyotis and Parastrellus (Hoofer & Van Den Bussche 2003).

Things have been improved since - the poorly resolved relationships within Vespertilioninae have been examined in several studies, and we now have a much tidier phylogeny. Roehrs et al. (2010) looked specifically at the relationships within and between vespertilionine 'tribes' and recovered the phylogeny you see - in, again, massively simplified form - below. Plecotins and lasiurins formed a clade, with the former paraphyletic to the latter (note that I haven't depicted this accurately: simplification and all that). Scotophilins and antrozoins were sister-groups. Perimyotis and Parastrellus - long regarded as pipistrelles - formed a clade informally dubbed the 'perimyotine group'; this was the sister-group to a large clade that included a 'mostly serotines' clade (whether the name Nycticeini or Eptesicini should be used for this clade remains unresolved), a 'hypsugine group' that included the Hypsugo 'pipistrelles' and kin, and Vespertilionini (Roehrs et al. 2010). This is the 'reference phylogeny' that we'll be coming back to again and again.

Agnarsson et al. (2011) generated an enormous phylogeny for all bats based on data from the cytochrome b gene [their main phylogeny is shown below: you can see that vesper bats take up a huge chunk of the tree on the left]; some aspects of their vesper bat topology are very similar to that recovered by Roehrs et al. (2010), but others are very different. To simplify in massive and unabashed fashion (and working 'up' from the bottom of the tree), they found a (Myotis + (Murinae + Kerivoulinae)) clade that was sister to remaining vesper bats. Among those "remaining vesper bats", 'core plecotins' grouped with serotines and kin, lasiurins grouped with antrozoins, and a clade that included both Vespertilio and most of the 'hypsugines' was sister to a noctule + 'true pipistrelles' clade. Scotophilins were outside the clade that included all the taxa just mentioned, as were the Cistugo species. Shock horror, bent-winged bats were nowhere close to vesper bats at all, but closer to noctilionids and phyllostomids (Agnarsson et al. 2011).

Unsurprisingly, there's a lot of work left to do on resolving vesper bat phylogeny - let alone work out where some of the enigmatic and fossil taxa go - but.... we do have the beginnings of a rough consensus.

Identifying vesper bats, and the phenomenon of cryptic species

There are many extremely distinctive vesper bat species, but there are also many extremely similar ones too - some only distantly related, yet superficially much alike in outward appearance. In the field, details of size, wing shape, foraging behaviour and flight style can be combined with the frequency and style of the bat's calls to make an identification, though you need lots of prior experience and (obviously) a bat detector for this to work [adjacent pic: your humble author with bat detector in hand. I belong to the Hampshire Bat Group].

But identifying some vesper bats to species level is often extremely difficult, even with the specimens in-hand. Closely related, similar species in a genus are often distinguished by details of tragus shape, tooth morphology and the proportional length of the calcar, tail tip and foot. The form of the baculum (penis bone) has proved useful in museum specimens. Subtle differences in morphology and differing call frequencies have led to the discovery that some vesper bat 'species' actually represent two or more so-called cryptic species: distinct, long-separate evolutionary units that look highly similar, but differ substantially in genetics and sometimes in ecology and behaviour.

The phenomenon of cryptic species in vesper bats first became well known following Baker's (1984) discovery of a new little yellow bat (Rhogeessa) that was morphologically near-identical, but chromosomally highly distinct, relative to other members of the group [adjacent photo: a species of little yellow bat, new to science as of 2008*]. This soon led to suggestions that "there may be numerous cryptic species of mammals that cannot be distinguished by classical systematic methods" (Nowak 1999, p. 447). Cryptic vesper bat species were later documented in Myotis, Plecotus, Pipistrellus and elsewhere (for more discussion see Hidden in plain sight: discovering cryptic vesper bats in the European biota). Cryptic species are not always exactly alike in morphology: careful work has shown that they can usually be distinguished when numerous measurements from different parts of the body are compared (Ashrafi et al. 2010).

* The name of the new species shown here was actually put up for auction. I don't know what the outcome was - let me know if you do.

In the several articles that'll follow this one I'm going to discuss the world's vesper bats - that's right, all of them (didn't I already say this?). Some of these bats will be familiar, but others definitely won't be, and as usual quite a few of them hardly ever get discussed in books, featured on television, or mentioned in any of the usual discussions about bats that one has at dinner parties, cocktail bars and so on.

On that note, where should you go if you want to learn a lot about the world's vesper bats? My first port of call for information on specific bats is always volume 1 of the essential Walker's Mammals of the World (Nowak 1999). Good news for bat-fans is that the bat section has actually been published on its own (Nowak 1994), though note that it's not as up-to-date as the sixth edition of Walker's Mammals of the World. For African vesper bats, Kingdon (1997) is useful. There are some good general texts on bat diversity, biology and behaviour: I recommend in particular Hill & Smith (1984) and Altringham (1999). One of my favourite books on bats is Russell Peterson's rather quirky Silently, By Night (Peter 1966).

For previous Tet Zoo articles in the vesper bats series, see...

And for previous Tet Zoo articles on bats, see...

• Desmodontines: the amazing vampire bats
• Giant extinct vampire bats: bane of the Pleistocene megafauna
• Camazotz and the age of vampires
• Dark origins: the mysterious evolution of blood-feeding in bats
• A new hypothesis on the evolution of blood-feeding: food source duality involving nectarivory. Catchy, no?
• Oh no, not another giant predatory flightless bat from the future
• The most terrestrial of bats
• I stroked a pipistrelle
• Red bats
• We flightless primates
• Big animalivorous microbats
• Hidden in plain sight: discovering cryptic vesper bats in the European biota
• PROTOBATS: visualising the earliest stages of bat evolution

Refs - -

Agnarsson I, Zambrana-Torrelio CM, Flores-Saldana NP, & May-Collado LJ (2011). A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS currents, 3 PMID: 21327164

Altringham, J. D. 1999. Bats: Biology and Behaviour. Oxford University Press, Oxford.

Ashrafi, S., Bontadina, F., Kiefer, A., Pavlinic, I. & Arlettaz, R. 2010. Multiple morphological characters needed for field identification of cryptic long-eared bat species around the Swiss Alps. Journal of Zoology 281, 241-248.

Baker, R. J. 1984. A sympatric cryptic species of mammal: a new species of Rhogeessa (Chiroptera: Vespertilionidae). Systematic Biology 33, 178-183.

Hill, J. E. & Harrison, D. L. 1987. The baculum in the Vespertilioninae (Chiroptera: Vespertilionidae) with a systematic review, a synopsis of Pipistrellus and Eptesicus, and the descriptions of a new genus and subgenus. Bulletin of the British Museum of Natural History (Zoology) 52, 225-305.

- . & Smith, J. D. 1984. Bats: A Natural History. British Museum (Natural History), London.

Hoofer, S. R. & Van Den Bussche, R. A. 2003. Molecular phylogenetics of the chiropteran family Vespertilionidae. Acta Chiropterologica 5, 1-63.

Kingdon, J. 1997. The Kingdon Field Guide to African Mammals. Academic Press, San Diego.

Koopman, K. F. 1994. Chiroptera: systematics. Handbook of Zoology: A Natural History of the Phyla of the Animal Kingdom 8 (60), 1-217.

- . & Jones, J. K., Jr. 1970. Classification of bats. In Slaughter, B.H. & Walton, D.W. (eds.). About Bats: a Chiropteran Biology Symposium. Dallas: Southern Methodist University Press, pp. 22-28.

McKenna, M. C. & Bell, S. K. 1997. Classification of Mammals: Above the Species Level. Columbia University Press, New York.

Nowak, R. M. 1994. Walker's Bats of the World. The Johns Hopkins University Press, Baltimore and London.

- . 1999. Walker's Mammals of the World, Sixth Edition. The Johns Hopkins University Press, Baltimore and London.

Peterson, R. 1966. Silently, by Night: About the Little-Known but Fascinating World of Bats. Longman, London.

Roehrs, Z. P., Lack, J. B. & Van Den Bussche, R. A. 2010. Tribal phylogenetic relationships within Vespertilioninae (Chiroptera: Vespertilionidae) based on mitochondrial and nuclear sequence data. Journal of Mammalogy 91, 1073-1092.

Simpson, G. G. 1945. The principles of classification and a classification of mammals. Bulletin of the American Museum of Natural History 85, 1-350.

Tate, G. H. H. 1942. Results of the Archbold expeditions. No. 47. Review of the vespetilionine bats, with special attention to genera and species in the Archold collection. Bulletin of the American Museum of Natural History 80, 221-297.

Van Den Bussche, R. & Hoofer, S. R. 2004. Phylogenetic relationships among recent chiropteran families and the importance of choosing appropriate out-group taxa. Journal of Mammalogy 85, 321-330.

Volleth, M. & Heller, K.-G. 1984. Phylogenetic relationships of vespertilionid genera (Mammalia: Chiroptera). Journal of Zoological Systematics and Evolutionary Research 32, 11-34.