Hypsugines: an assemblage of 'pipistrelle-like non-pipistrelles' (vesper bats part XV)

As we've seen throughout this series (see links below for previous parts), recent phylogenetic studies have found a number of 'pipistrelle-like non-pipistrelles' to form a novel clade previously unsuspected from morphological studies [composite above shows - l to r - Hypsugo cf. joffrei (from Kruskop & Shchinov (2010)), Neoromicia capensis (from Fernloof Nature Reserve), and Laephotis botswanae]. Following Roehrs et al. (2010), I'll refer to this as the 'hypsugine group'. Hypsugines occur across the Old World and Australasia, and at the 'core' of the group are the Hypsugo species.

There are about 18 of these superficially pipistrelle- or noctule-like bats; they're known from southern Europe, much of Asia and most of Africa and Madagascar. Their detailed anatomy reveals that they are indeed very different from pipistrelles proper, possessing myotodont lower molars (pipistrelles have nyctalodont lower molars) and a short, robust baculum (that of pipistrelles is long and slender: look at the figure in the serotine article) (Kruskop & Shchinov 2010) [see figure below, from Kruskop & Shchinov (2010)].

The best known Hypsugo bat is Savi's bat H. savii [shown right down at the bottom], known until recently as Savi's pipistrelle. It occurs across southern Europe, continental Asia, north-west Africa and the Canary and Cape Verde Islands. It used to occur in Germany but now seems locally extinct; it occurs as an occasional vagrant as far north as the UK, and its presence is suspected but not yet confirmed in such places as Armenia, Bhutan and various of the former Yugoslavian countries.

In the 1990s it was shown that Savi's bat is highly variable in coat colour [adjacent photo shows variation; from Arlettaz et al. (1993)]. Most individuals have bicoloured hairs, where the base is dark and the tips are blonde or gold, but as many as a quarter of the bats in some populations are uniformly blackish, and greyish specimens have also been discovered (Arlettaz et al. 1993).

This phenotypic variation far exceeds that seen in other European bats. Immediately it raises the suspicion that Savi's bat is a complex of cryptic species, but so far it seems that this variation represents polymorphism - whether it has any selective advantage remains to be determined so far as I can tell (it could perhaps represent random drift of a selectively neutral character).

The precise contents of Hypsugo are as yet unresolved: bacular morphology and genetics indicates that some of them (like H. nanus) should be moved to another hypsugine genus, Neoromicia (Kearney et al. 2002). You might remember from the nycticein article that Schlieffen's bat Nycticeinops schlieffenii seems to be a hypsugine. Helbig et al. (2010) found Schlieffen's bat to be nested within Hypsugo. To avoid a paraphyletic Hypsugo, they therefore suggested that the African Hypsugo species at least should be referred to Nycticeinops... but it has to be the other way round, since Hypsugo was named in 1856 while Nycticeinops didn't appear until 1987. This mess has yet to be sorted out: people who dislike name changes will not be pleased, but do remember that we're at but early stages in our understanding of the affinities of these bats.

Vespadelus and the falsistrelles

The six or so Australian Vespadelus species (sometimes called 'cave bats' - what a great name!) were recovered as the sister-group to the Australasian lobe-lipped bats (Chalinolobus)* by Roehrs et al. (2010) and Agnarsson et al. (2011); in turn, the clade formed by these two was recovered as the sister-group to Hypsugo. The Vespadelus bats were typically included in the serotine genus (Eptesicus) or within Pipistrellus. Agnarsson et al. (2011) referred to the one Vespadelus species in their database as Eptesicus regulus; this explains (in part**) why Eptesicus appears non-monophyletic in their tree [V. vulturnus shown here, from Young & Ford (1998)].

* They're not discussed in this article, despite being hypsugines. Patience :)

** They also found E. nasutus to group well away from the rest of Eptesicus and in a sister-group relationship with the Western pipistrelle/Canyon bat/American parastrelle Parastrellus hesperus (discussed in the perimyotine article).

Little is known about these bats. At least some of them are known to prefer large, old, hollowed trees as roost sites, preferably with little surrounding vegetation. A sample of V. vulturnus specimens had a mean mass of 3.2 g, making this Australia's smallest mammal and one of the tiniest in the world (Young & Ford 1998). As is typical for vesper bats, females are somewhat bigger than males.

Falsistrellus, the five or so false pipistrelles or falsistrelles, might be close relatives of Vespadelus (Volleth & Heller 1984) and hence also part of the hypsugine clade. Native to Australia as well as India, south-east Asia, Indonesia, Sulawesi and the Philippines, falsistrelles were long considered to be pipistrelles in the strict sense. Troughton's (1943) suggestion that they should be regarded as separate has proved increasingly popular: like the other pipistrelle-like taxa discussed here, they now seem to be but distant relatives of pipistrelles proper. Little is known about falsistrelles; a distinctive morphological character is the presence of an especially tiny second upper incisor. In the Eastern falsistrelle F. tasmaniensis [head shown here, from Parnaby (1992)], Parnaby (1992, p. 26) described it as "a small splint scarcely protruding from the gum".

Neoromicia and Laephotis

Also apparently part of the hypsugine clade are the Neoromicia species. These were included within Pipistrellus until Hill & Harrison (1987) proposed that they should be distinguished from them (at 'subgeneric' level) on the basis of bacular morphology. Several studies (Kearney et al. 2002, Stadelmann et al. 2004, Roehrs et al. 2010, Agnarsson et al. 2011) have found the Neoromicia bats to be paraphyletic with respect to the tropical long-eared bats or African long-eared bats (Laephotis), a group of species that I, very much unwisely, included in the plecotin article. The paraphyly observed within Neoromicia has led some workers to propose that at least two Neoromicia - N. capensis and N. somalicus - should be transferred to Laephotis (Helbig et al. 2010).

While based on molecular data, this assignment is also supported by bacular morphology: the baculum in Laephotis is about identical to that of the Neoromicia species N. capensis and to a population referred to as N. cf. melckorum (Kearney et al. 2002). Strangely, the baculum has a long, anteroventrally projecting process in both these Neoromicia species and in Laephotis - I'm really not sure what this means for the shape of the penis in the live animal [diagram below - from Kearney et al. (2002) - shows baculi of various vesper bats. Species of Hypsugo, Neoromicia and Laephotis are shown at the bottom. Note the weird shapes obvious in the lateral views].

Variously classified by previous authors among pipistrelles or serotines (the type species is Eptesicus zuluensis Roberts, 1924), the approximately 12 Neoromicia species range throughout tropical Africa and Madagascar, and the species that have common names are generally still referred to as 'pipistrelles' or 'serotines', depending on body size. They occur throughout forests and grasslands of various kinds. Most species are predominantly light brown in coat colour, but N. rueppellii has bright white ventral and lateral surfaces. The generic name Neoromicia is feminine, so there's been a push to get the relevant species names converted to the right gender (Riccucci & Lanza 2008).

Coming next: quite possibly more bats. More than 6000 visitors every day can't be wrong! [Savi's bat shown here; image by Monika Podgorelec, from wikipedia].

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

• Introducing the second largest mammalian 'family': vesper bats, or vespertilionids
• The vesper bat family tree: of myotines, plecotins, antrozoins, and all those cryptic species (vesper bats part II)
• Bent-winged bats: wide ranges, very weird wings (vesper bats part III)
• Of southern African wing-gland bats, woolly bats, and the ones with tubular nostrils (vesper bats part IV)
• The many, many mouse-eared bats, aka little brown bats, aka Myotis bats (vesper bats part V)
• Long-eared bats proper: Plecotus and other plecotins (vesper bats part VI)
• Desert long-eared bats - snarling winged gremlins that take scorpion stings to the face and just don't care (vesper bats part VII)
• Hairy-tailed bats: a tale of furry tails, red coats, cold tolerance, migration and sleeping out in the open (vesper bats part VIII)
• Robust jaws and a (sometimes) 'greenish' pelt: house bats (vesper bats part IX)
• Australasian big-eared bats, and how to (perhaps) single-handedly wipe out an entire species, 1890s-style (vesper bats part X)
• Antrozoins: pallid bats, Van Gelder's bat, Rhogeessa... Baeodon!! (vesper bats part XI)
• Putting the 'perimyotines' well away from pips proper (vesper bats part XII)
• Nycticein bats: apparently, a nice example of how assorted distant relatives can be mistakenly considered close allies on the basis of one or two characters (vesper bats part XIII)
• Eptesicini: the serotines and their relatives (vesper bats part XIV)

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, C. M., Flores-Saldana, N. P. & May-Collado, L. J. 2011. A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Currents 011 February 4; 3: RRN1212. doi: 10.1371/currents.RRN1212.

Arlettaz, R., Guibert, E., Lugon, A., Médard, P. & Sierro, A. 1993. Variability of fur coloration in Savi's bat Hypsugo savii (Bonaparte, 1837). Bonn. Zool. Beitr. 44 (3-4), 293-297.

Helbig, M., Datzmann, T., Mayer, F. & Fahr, J. 2010. Molecular phylogeny of African "pipistrelle" bats (Vespertilionidae) suggests new clades, rearrangement of genera, and extensive cryptic diversity within species. African Bat Conservations News 23, 36-37.

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.

Kearney, T. C., Volleth, M., Contrafatto, G. & Taylor, P. J. 2002. Systematic implications of chromosome GTG-band and bacula morphology for southern African Eptesicus and Pipistrellus and several other species of Vespertilionidae (Chiroptera: Vespertilionidae). Acta Chiropterologica 4, 55-76.

Kruskop, S. V. & Shchinov, A. V. 2010. New remarkable bat records in Hoang Lien Son mountain range, northern Vietnam. Russian Journal of Theriology 9, 1-8.

Parnaby, H., 1992. An interim guide to identification of insectivorous bats of south-eastern Australia. Technical Reports of the Australian Museum 8, 1-33.

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.

Riccucci, M. & Lanza, B. 2008. Neoromicia Roberts, 1926 (Mammalia Vespertilionidae): correction of gender and etymology. Hystrix 19, 175-177.

Stadelmann, B., Jacobs, D. S., Schoeman, C. & Ruedi, M. 2004. Phylogeny of African Myotis bats (Chiroptera, Vespertilionidae) inferred from cytochrome b sequences. Acta Chiropterologica 6, 177-192.

Troughton, E. Le G. 1943. Furred Animals of Australia. Angus and Robertson:, Sydney.

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

Young, R. A. & Ford, G. I. 1998. Range extension of the Little forest bat Vespadelus vulturnus (Chiroptera: Vespertilionidae) into a semi-arid area of central Queensland, Australia. Australian Zoologist 30, 392-397.