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.
The form of the baculum (penis bone) has proved useful in museum specimens.
This left me with the (undoubtedly grossly inaccurate) mental image of the males having a much harder time telling whether females are conspecifics than vice versa.
mentioned in any of the usual discussions about bats that one has at dinner parties, cocktail bars and so on.
Evidently I don't get invited to the right sort of parties.
This suggests a really messy tangle at that little ol' junction between genetics, ecology, and morphological taxonomy.
We've either got the best example of mammalian convergence I've ever seen in my life, or there's something about that concept of niche theory that isn't making a huge amount of sense. And when there are species that are chromosomally distinct but morphologically near identical...what can I say?
Actually, this sounds like the mess we botanists have to deal with, because plants can go autopolyploid with a single mitotic failure. Seeing this kind genome vs. morphology vs. ecology confusing in mammals is a both unsettling and amusing. Better go talk to the botanists, and see how they've dealt with it.
@Andreas: I think they are focusing on the baculum because no one has thought to preserve female bat genitalia. If they did, I suspect they'd see as much diversity there, just as they did in ducks.
Well, there's 'morphologically near identical' and there's 'morphologically near identical'. The species concerned might look much alike in outward appearance, but be much different on the insides (in which case, those similarities are superficial). I didn't mean to imply that distant relatives are near-identical phenotypically. In fact - out of interest - what made you think that I was saying this?
as up-to-date as the sixth edition of Walker's Mammals of the World
That's damning with faint praise IMO... Dear Johns Hopkins University Press people: can we please, please get a seventh edition of WMotW?! And if we do, please let it be an edition worthy of the 21st century: replace those ancient black-and-white pictures of zoo specimens (or stuffed skins!) with colour photographs of wild animals, update the obsolete taxonomy (e.g., 'order Pinnipedia' - ugh!), and return to a three- (or even four-)volume format.
I know, I know; in all likelihood, none of the above is ever gonna happen. *sulks*
Fascinating stuff - back in the day (i.e. as an undergraduate when Yalden & Morris's 'Lives of Bats' was the book to have) it looked like I might go down the bat-research route, but here I am focusing on entomology (via chalk grassland eology & limnology) which Darren might consider to be 'bat-food studies' *grin*
"You'll definitely want to skip this whole article if identifying clades and phylogenetic branching patterns bores you to tears ."
Heh, right. We're readers of Tetrapod Zoology, right?
Heck I'll bet about half of us come here for the phylogeny/taxonomy p/o/r/n/ ah... information.
Can't get this stuff anywhere else, keep up the good work.
"update the obsolete taxonomy (e.g., 'order Pinnipedia' - ugh!)"
googling "pinniped phylogeny" as a layperson, it looks to me like Pinnipeds are supported, e.g.
What am I missing?
David (Houston): thanks much for kind comments :)
As for Pinnipedia, Dartian is probably referring to the fact that Nowak has Pinnipedia as if it's a separate 'Order' relative to the rest of Carnivora. For some of the editions (e.g., the sixth) this even means that Pinnipedia is in a separate volume from the rest of Carnivora.
One other comment on big, total-mammal volumes: volume 1 of Lynx Edicions' Handbook of the Mammals of the World has been out since 2009. Still I haven't seen it - to those who have, what's it like? Sigh, I so need to be rich.
As for Pinnipedia, Dartian is probably referring to the fact that Nowak has Pinnipedia as if it's a separate 'Order' relative to the rest of Carnivora.
Precisely that. Phylogenetically, pinnipeds* are nested well within caniform carnivores; by the time of publication in 1999, that had already been established beyond any reasonable doubt. Nowak really had no good excuse to use such 'folk taxonomy' anymore. (Nor did he have any phylogenetically defensible excuse to place, as he did, humans in the family Hominidae and all the other great apes in the family Pongidae.)
* Lest there be any misunderstanding: Pinnipedia is almost certainly a real, monophyletic clade (though there were some doubts about that as recently as a few decades ago). But the point is that you can't treat it as an 'order' - like Nowak did - unless you either are prepared to accept rampant paraphyly in your classification schemes, or are willing to also elevate many/most of the traditional terrestrial carnivore 'families' to 'order' level.
Darren: I have HMW Vol 1. Didn't have to pay for it (I'd rather not explain). It was a bit of disappointment compared to HBW. No critical re-evaluation of subspecies (and no description of inter-subspecific differences in most cases), lots of errors, questionable taxonomic decisions with no reason given. Also, I have a growing suspicion that small mammal volumes (which are the most valuable ones as there's more than enough info on large mammals) are going to be lousy jobs. But it's a bit cheaper than HBW, at least for now.
Thanks indeed, Vlad... opinion much appreciated (and I must say that I'm a bit disappointed). I agree (and have always said) that there's a dire need for good, comprehensive volumes on the small, obscure (but phenomenally speciose) groups - rodents and bats among mammals - the problem is that the market is small, so no incentive to pour time and money into such projects.
Speaking of projects, are you familiar with mammalwatching.com? It's a bit small for now, but I think it has good potential - I already use it for every trip.
a real, monophyletic clade
I'd better correct that before David M. sees it... I should have written 'a real, monophyletic taxon' - clades are, of course, by definition monophyletic.
Selected bats and other mammals are avialable here:
Mammalian Species Accounts and Links to PDFs
Rather surprisingly, much of the old information is still accurate - which reflects how little has been done on many mammals at all.
I'd better correct that before David M. sees it...
I was actually willing to let it slip here. Emphasis by repetition (arguably, "real" is up there with "monophyletic": arguably, clades are either real or don't exist at all) is a well-established figure of rhetorics. :-)
@Dartian and Darren.
Right, of course, pinnipeds are in carnivora. I wasn't thinking clearly there. There is enough stuff, though, recently that massively rearranges trees that I misread the comment to mean that they weren't monophyletic.
Thank you for the correction and amplification.
Cladistics changed the tradition taxonomy of Carnivora because Pinnipedia is monophyletic, but Fissipedia isn't, since pinnipeds are nested in Arctoidea subdivision of Caniformia.
I have volume 1 of handbook of mammals of the world, and rather liked it. Bear in mind that I have only superficially looked at the handbook of birds of the world. It however does have illustrations for just about every carnivoran mammals species known, and appears to be pretty up to date. I have heard though of other people being disappointed in it.
I also worry how the rodent and bat volumes will turn out. Compressing information on 1000 species of bats into one volume means something has to give.
"Bat detector" sounds like something Calvin (of Calvin and Hobbes) would love to have had, especially since he though bats were giant bugs.
You'd get more 'discussions about bats that one has at dinner parties, cocktail bars and so on' if you carried your bat detector around with you. When asked what it is, say 'Bat detector. You can never be too careful!' and there's your conversation off to an intriguing start.
I once recorded bat noises directly from a bat detector onto my mobile phone and thus carry a set of bat noises around with me all the time (as well as sound-bites from Hoover the talking seal and various other bits of miscellany). I therefore frequently amuse like-minded people with bursts of bat chatter. I can assure you that this does indeed go down well at any social function. Just like the muntjac skull I was given in a pub over the weekend.
volume 1 of Lynx Edicions' Handbook of the Mammals of the World has been out since 2009. Still I haven't seen it
I haven't seen it either, but after having read about this book series on the Lynx Edicions' homepage I'm no longer sure that I want to.
First off: Vladimir and Morgan are quite right in pointing out that the decision to cram all the bats and all the rodents (presumably together with the lagomorphs) into their single respective volumes was probably not a good one. Lynx Edicions could have avoided this problem by arranging the material in HMW in the same running-order way as they did in the widely-acclaimed HBW.
But my main issue with this book series is its outrageously oldfashioned phylogenetic layout. The Carnivores volume excludes pinnipeds. The Hoofed Mammals volume will include various afrotherians as well as the frikkin' pangolins. There will be a Sea Mammals volume. (Sheesh, why not have a Large Mammals or a Long-tailed Mammals volume too? That would make as much - or as little - sense.) The contents of the Insectivores volume have not yet been revealed, but - by default - they are bound to be the usual wastebasket hodgepodge of various totally unrelated invertebrate-eating placentals.
All that makes an utter mockery of the claims that the books will "provide up-to-date information on the systematic relationships" and "present the taxa in phylogenetic sequence, which reflects the evolutionary relationships as we currently understand them". The editors of HMW aren't even bound by tradition in the same way that a publication such as Walker's Mammals of the World arguably is - they were effectively starting from a clean slate and could thus easily have embraced the results of modern phylogenetic research in mammalogy. But for reasons that are hard to fathom (for yours truly anyway), they did not.
Sorry for ranting, but I strongly feel that publications of this kind have a special opportunity (and indeed a responsibility) to educate their readers in current scientific thinking. It seems to me that HMW has missed that opportunity pretty badly.
Ok, fair enough, Dartian. But - - I think I first heard mention of this planned series years and years and years ago, seriously - I mean, back in the previous century. If that's right, then it's certainly possible that the editors submitted a synopsis/volume plan prior to the publication of many of the recent phylogenetic proposals you have in mind (or, perhaps prior to those editors becoming aware of these proposals, at least). Of course, even if this is true, you could argue that they should have modified any plan accordingly. Do note, however, that things in publishing are hard to modify once they get moving, especially when lots of people are involved (I speak from bitter experience).
As a complete stranger to the world of bats, I have to ask, with such a plethora of morphologically distinguishable specimens, how can you ever decide where to draw species boundaries?