University of Western Ontario

Biology 3224a

BIOLOGY OF BATS

Phylogeny & Evolution

This presentation consists of xx slides

1

How should we interpret structural similarity among species?

Tubular nostrils

Paranytctimene Murinaraptor leucogaster

Naked-backed bats

Dobsonia moluccensis Pteronotus davyi

Megaloglossus

Choeronycteris

Flower-visiting bats

Neoplatymops Platymops Sauromys Tylonycterismattogrossensis setiger petrophilus robustula

Flat-headed bats

Classification should reflect evolutionary history. One step is to describe the organisms, in our case bats. Arrange them in a hierarchy (species, genus, family, etc.) and then determine whether or not the hierarchy reflects evolutionary history. This is much easier (or more difficult) if there is a fossil record.

The challenge … how to recognize parallel and convergent evolution.

The resolution … answer the question, did the common ancestor have the trait(s)?

Simmons & Geisler(1998) presented Dobson’s (1875) view.

People have wondered and speculated about the situation in bats.

Jepsen (1966) described Icaronycteris index, an Eocene bat fossil from Wyoming (Green River Formation).

Jepsen (1970) followed this up with some reflections about the evolution of bats --- suggested that they evolved in caves.

From Simmons and Geisler1998

From Jones & Teeling2006

One of the first comprehensive looks at the phylogeny of bats is provided by Simmons and Geisler (1998). This important paper also took into account a variety of fossil bats, including some from the Eocene.

Simmons and Geisler (1998) present several phylogenies and the ones arising from their analyses are supported by appropriate statistic.

But before we delve into phylogeny, we must address the question “are bats monophyletic?” Today the prevailing view is “yes”, but that is not a unanimous view and not the one that was under discussion in the 1980s and 1990s.

Simmons & Geisler 1998

Smith’s 1976 phylogenies redrawn and published in Simmons and Geisler (1998).

Van Valen’s1979 take on the topic – from Simmons and Geisler 1998.

Smith and Madkour 1980

Smith and Madkour (1980) used a variety of penialcharacters to support the view that bats (Chiroptera) were diphyletic.

In other words Megachiroptera have a different origin than Microchiroptera.

Smith and Madkour 1980

Synapomorphies = black bars, shared derived characters

Smith and Madkour 1980

Synapomorphies = black bars, shared derived characters

Enter J. D. (Jack) Pettigrew.

He used electrophysiological and neuroantomical methods to discover that the pattern of connections between the retina and midbrain differed between the Megachiroptera and the Microchiroptera. The Megachiroptera had an advanced retinotectalpathway previously known only from Primates.

The ancestral condition (symplesiomorphous) of retinotectalconnections occurs in the Microchiroptera and in all other vertebrates.

In 1991 most of an issue of Systematic Zoology was dedicated to the question of monophyly in bats.

Pettigrew 1991

Pettigrew (1991) laid out four scenarios for the evolution of bats (= flight in mammals).

Pettigrew 1991

Pettigrew 1991

Baker et al. 1991

Baker et al. (1991) presented it slightly differently.

Baker et al. 1991

Pettigrew 1991

Baker et al. 1991

Baker et al. 1991 …a phenetic view

Baker et al. 1991

Baker et al. 1991, a cladistic view

Baker et al. 1991

Baker et al. 1991

By 1994, most biologists informed about the situation agreed that Chiroptera were monophyletic. Simmons (1994) summarized the situation. Jack Pettigrew remains unconvinced (I think).

If Chiroptera are monophyletic, then the retinotectal pathway similarities between Primates and Pteropodidae represents a convergence.

Simmons and Geisler(1998) presented the results of a phylogeneticanalysis with 195 morphological features and 12 rDNA(restriction sites) features. Considered digital and multistate features.

Consensus tree from 208 discrete features.

Decay values/ bootstrap values

Since 1998, further analysis, including a growing genetic data base, support monophyly of living bats but the classification has changed dramatically.

Megachiroptera and Microchiroptera are no longer valid terms, replaced by Yinpterochiroptera and Yangochiroptera.

Jones & Teeling 2006

The situation today. Yinpterochiropteraand Yangochiropterabecome suborders.

Jones & Teeling 2006

Make the comparison … new and old

Teeling (2009) outlines four alternatives.

Teeling 2009

Echolocation an ancestral condition

Echolocation evolved four times in bats

Teeling 2009

W = wings

S = laryngeal echolocation

P = primate features

A = archontan skeletal features

--- = loss

Recall from Pettigrew 1991

Jones & Teeling 2006

The situation today. Yinpterochiropteraand Yangochiropterabecome suborders.

What next?

FoxP2 is the “mammalian vocalization gene. Mice without this gene do not produce isolation calls. Li et al. (2007) looked at this gene in a variety of bats. FoxP2 is extremely diverse in echolocating bats … but not enough information to determine if pteropodids had had and then lost the ability to echolocate.

Li et al. (2008) then looked at the “hearing gene” Prestin. Prestinis said to be the cochlear amplifier .. Encodes transmembranemotor proteins that drive electromotility of outer hair cells. Two different phylogenetic signals in the data.

Analyses of entire coding region suggests echolocating bats are monophyletic.

Phylyogenetic analyses of amino acids found in transmembrane regions alone supported the current phylogeny (Yinpterochiroptera and Yangchiroptera).

Bottom line, no clear answer.

Eick et al. 2005 presented another analysis … same picture pretty much …bit there are some important differences. Note the Laurasiatheiaconnections. Vertical arrows indicate unique indel events supporting phylogeneticassociations.

Teeling 2009

Echolocation an ancestral condition

Echolocation evolved more than once (perhaps four times) in bats

What is the essence of a bat?

WINGS

When did they appear? 60 million years ago (at least)

Why did they appear?

What are convergent characters?

What are parallel characters?

Perhaps the current view brings classification and evolutionary history into closer agreement.

Onychonycterisfinneyi … could it echolocate?

Simmons et al. 2008.

Literature CitedArita, H.T. & M.B. Fenton. 1997. Flight and echolocation in the ecology and

evolution of bats. Trends in Ecology and Evolution, 12:53-58.Baker, R.J., M.J.Novacek and N.B. Simmons. 1991. On the monophyly of bats.

Systematic Zoology, 40:216-231.Dobson, G.E. 1875. Conspectus of the suborders, families and genera of

Chiroptera arranged according to their natural affinities. Annals of theMagazine of Natural HIstory, Series 4, 16:345-357.

Eick, G.N., D.S. Jacobs, and C.A. Matthee. 2005. A nuclear DNA phylogeneticperspective on the evolution of echolocation and historical biogeography of extant bats (Chiroptera). Molecular Biology and Evolution, 22:1869-1886.

Fenton, M.B., D. Audet, M.K. Obrist & J. Rydell. 1995. Signal strength, timing andself-deafening: the evolution of echolocation in bats. Paleobiology, 21:229-242.

Li, G., J. Wang, S.L. Rossiter, G. Jones and S. Zhang. 2007. Accelerated FoxP2evolution in echolocating bats. PLOS One, September 2007, Issue 9, e900.

Li, G., J. Wang, S.J. Rossiter, G. Jones and S. Zhang. 2008. The hearing genePrestin reunites echolocating bats. Proceedings of the National Academy of Science, Washington, 105:13959-13964.

Jepsen, G.L. 1966. Early Eocene bat from Wyoming. Science, 154:1333-1339.Jepsen, G.L. 1970. Bat origins and evolution, pp. 1-64. IN Biology of bats (W.A.

Wimsatt, Editor). Academic Press, Volume 1Jones, G. and M.W. Holderied. 2007. Bat echolocation calls: adaptation and

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Pettigrew, J.D. 1991. Wings or brain? Convergent evolution in the origins of bats.Systematic Zoology, 40:199-216.

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

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

Simmons, N.B., K.L. Seymour, J. Habersetzer and G.F. Gunnell. 2008. Primitiveearly Eocene bat from Wyoming and the evolution of flight and echolocation.Nature, 451:818-821.

Simmons, N.B. and J.H. Geisler. 1998. Phylogenetic relationships ofIcaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx toextant bat lineages in Microchiroptera. Bulletin of the American Museum of

Natural History, 235:1-182. Smith, J.D. 1976. Chiropteran evolution, pp. 49-69 IN Biology of bats of the New

World family Phyllostomatidae (R.J. Baker, J.K. Jones Jr. and D.C. Carter –editors). Texas Tech University Press, Lubbock.

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Tabuce, R., M.T. Antunes and B. Sige. 2009. A new primitive bat from the earliestEocene of Europe. Journal of Vertebrate Paleontology, 29:627-630.

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Van Valen, L. 1979. The evolution of bats. Evolutionary Theory, 4:104-121.