1. Pettigrew, J.D. (1986) Flying primates? Megabats have the advanced pathway from eye to midbrain. Science, 231: 1304-1306.
This is the paper that re-started the old controversy about bat-primate relationships:-
Flying foxes* have a striking
pattern of projection from the retina to the midbrain that is not found
in any mammalian Order except primates, for which it was thought to be
a diagnostic character. Even the most highly-visual microbats (e.g. Macroderma
gigas) lack this pattern of retino-tectal connections, raising the
possibility that an early branch of primates evolved flight independently
of the microbats.
2. Pettigrew, J.D. and Jamieson, B.G.M. (1987) Are flying foxes really primates? Aust. Mammal., 10, 119-124.
A cladistic analysis of brain
traits that supports the flying primate hypothesis
3. Pettigrew, J.D., Dreher, B., Hopkins, C.S, McCall, M. J. and Brown, M. (1988) Peak density and distribution of ganglion cells in the retinae of microchiropteran bats: Implications for visual acuity. Brain Behav. Evol. 32: 39-56.
Shows the range of visual abilities of microbats and the dramatic contrast with the visual system of flying foxes. As well as having lower acuity, microbats have an inverted position of the horizontal streak when compared with most other mammals, including flying foxes. This paper also establishes the range of visual ability amongst microbats and therefore the validity of comparisons between the ghost bat (with the highest visual acuity of any microbat) and flying foxes. The ghost bat has the most highly-developed visual system, with the largest number of retinal ganglion cells, of any microbat. One can therefore argue safely that visual specialisations that were found to be absent from ghost bats are unlikely to turn up in Amorphochilus, Furipterus or some other rare, non-visual microbat .
4. Pettigrew, J.D., Jamieson, B.G.M., Hall, L.S., Robson, S. R., McAnally, K.I. and Cooper, H.M. (1989) Phylogenetic relations between microbats, megabats and primates (Mammalia: Chiroptera and Primates) Phil. Trans. Roy. Soc. B. 325: 489-559.
This long treatise sets out the evidence for the flying primate hypothesis as it was in 1989. More brain characters shared between primates and flying foxes and primates are added to the case in a cladistic analysis that supports an origin of flying foxes from primate ancestry, with a much earlier origin of microbats. A new wing character, the ratio of metacarpal to phalanx lengths, splits the bats into two sets without overlap, playing havoc with the case that flying foxes and microbats must be related because of similarities in the wings. Protein sequence data from haemoglobin, while not resolving the issue, are consistent with polyphyletic origins of bats and presage the difficulties with the interpretation of molecular data that are to come.
5. Pettigrew, J.D. (1990) Flying lemurs and other animals. Nature 346:520
The colugo, or gliding lemur,
occupies a key position in discussions about evolution because it is the
only living mammal with a gliding membrane (patagium) that encloses all
digits and therefore might represent a precursor to a bat. The brain data,
behaviour, reproductive system, as well as corollaries of the "flying primate"
hypothesis, all support a special link between colugos and flying foxes,
but not between colugos and microbats.
6. Pettigrew, J.D. (1991) Wings or brain? Convergent evolution in the origins of bats. Systematic Zoology 40: 199-216
7. Pettigrew, J. D. (1991) A fruitful wrong hypothesis? Systematic Zoology 40:231-239
These papers are part of a 4-part
debate on the controversy that was invited by the editor of Systematic
Biology. While there are a few cheap shots from both sides, the debate
shows how widely the flying primate hypothesis has impinged on different
aspects of biology, including:- the use of brain characters to infer phylogeny;
cladistics; molecular phylogeny; evolutionary biology and the origins of
flight;
8. Rosa, M.G.P, Schmid, L.M., Krubitzer, L.A. and Pettigrew, J.D. (1993) Retinotopic organisation of the primary visual cortex of flying foxes (Pteropus poliocephalus and Pteropus scapulatus). J. Comp. Neurol. 331:1-18
Establishes more bona fides
for the highly developed visual system of the flying fox in comparison
to all other mammals, especially microbats. Flying foxes are shown to lie
with primates, and away from all other mammals, on a plot of visual cortex
size vs. body size.
9. Rosa, M.G.P., Schmid, L.M. and Pettigrew, J.D. (1994) Retinotopic organisation of the Second Visual Area, in the Megachiropteran Bat (Pteropus ). Cerebral Cortex 4: 52-68
Helps to define quantitatively
the boundary between carnivores and primates when the visual system is
used. Flying foxes are clearly closer to primates than are carnivores (microbats
would not even make it onto the graph with their tiny visual cortex).
10. Rosa, M.P. and Schmid, L.M. (1994) Topography and extent of visual field representation in the superior colliculus of the megachiropteran Pteropus. Visual Neuroscience 11: 1037-1057
This paper deals quantitatively with the details of the flying fox retinotectal pathway, confirming with electrophysiology that it has the primate pattern of sparing the ipsilateral hemifield. The decussation between hemifields is not so precise in flying foxes as it is in anthropoid primates, raising the possibility in some minds that it was more like the pattern in carnivores than in primates. This work shows that the flying fox pattern is truly primate-like and much closer quantitatively to primates than is the pattern in carnivores (such as the cat, which have the most primate-like pattern of any mammal, but which still have an input from the ipsilateral hemifield). Note that the understanding of retinotectal pathways in lemurs and tarsiers is poor; we should not expect them to have such precise retinotectal decussations as anthropoids, so flying foxes may well prove to lie exactly with primates at this level of quantitative detail, just as happens with quantitative data on primary visual cortex (see 8 above).
This paper also discusses the
apparent contradiction with a similar study of the smaller, cave-roosting
megabat, Rousettus which did not find a clear hemi-decussation of
the retino-tectal pathway. One technical difference between the studies
was the angle of the head in the frame used for recording. In the study
of Rousettus the head was angled horizontally, so the visual axis
would have been angled upwards, permitting exploration only of the inferior
field where the decussation is more diffuse.
11. Buhl, E.H. and Dann, J.F. (1991) Cytoarchitecture, neuronal composition, and entorhinal afferents of the flying fox hippocampus. Hippocampus, 1: 131-152
Since many of the intially-described neural characters shared between flying foxes and primates were visual, it has been argued by opponents of the flying primate hypothesis that they may have been acquired independently in the two lines because of selective pressures common to a highly-visual lifestyle. This argument has weakened with the discovery of numerous other neural features shared by flying foxes and primates that cannot be accounted for in this way. Such characters include features of cortical organisation (see 7 & 8), as well as the hippocampal features described in this paper.
12. Pettigrew, J.D. (1994) Flying DNA . Current Biology 4: 277-280
This paper deals with the mutational biases toward higher levels of AT that have appeared in the DNA of homeotherms like birds and mammals. The relevance of this mutational bias to the flying primate debate is that it seems to be greatest in bats, raising the possibility of convergent similarity in the DNAs of these highly metabolic creatures. This possibility is supported by the fact that the substitutions claimed in support of the monophyly of bats are largely A or T substitutions. One must therefore rule out the possibility that the shared AT bias seen in the DNA of the two kinds of bats was acquired independently, as flight may have been, rather than present in a common flying ancestor. Analysis that corrects for the AT bias, such as protein sequence data, or of G and C substitutions only, supports the flying primate hypothesis.
13. Rosa, M.P.G., Pettigrew,J.D. and Cooper, H.M. (1996) Unusual pattern of retinogeniculate projections in the controversial primate, Tarsius. Brain Behavior and Evolution 48:121-129
This paper shows that some fundamental aspects of primate phylogeny are still imbedded in controversy. The tarsier is an undoubted primate, but to which major branch of the primate tree does the tarsier belong? Popular view has the tarsier aligned with anthropoids, but this paper presents neural data in support of a completely different view:- viz. that the tarsier is the living representative of the oldest lineage of primates and that it is therefore paraphyletic to all other living primates. The importance of the paper in the light of flying primate hypothesis is threefold:-
i. primate relationships are still in flux, so one should not be too surprised to find new viewpoints on possible sister taxa such as flying foxes.
ii. this new information on a basal primate is crucial for understanding the relationships of primates to sister taxa, since it is only the basal characters shared by all primates that can be validly used to compare them to sister taxa.
iii. the tarsier shares derived
characters with the colugo, (a controversial possible relative of both
flying foxes and primates), that it does not share with any other primate,
thereby emphasising the complex basal radiation of early primates from
which the flying foxes may have arisen.
Recent molecular evidence provides support for the phylogenetic position of Tarsius, paraphyletic to other primates, that is forced by these brain data. The clearly basal position occupied by Tarsius in these DNA and protein sequence studies (12SRNA and apha-crystallin) is in clear conflict with the "Tarsius is an anthropoid" point-of-view that dominates. I highly recommend this issue as one to watch, since the emerging molecular data are congruent with the brain data, whilst both are at odds with prevailing wisdom. The power of the brain data to provide a completely new insight is evident....and appropriate given that primates are largely characterised by derived aspects of brain and behaviour. I think that the brain data on "flying primates" are equally powerful and note that their is increasing support from molecular studies that take into account the unusually large amount of modification of the flying fox genome.
14. Pettigrew, J.D. and Kirsch, J.A.W. (1995) Flying primates revisited: DNA hybridisation with fractionated, GC-enriched DNA. South African Journal of Science 91: 477-482
A rather colloquial summary of the case in 1995, taken from the transcript of a talk at Robinson's Fectscrift. Has some data that one will not find summarised in this way elsewhere (e.g. fossil record of the 2 kinds of bats. )
15. Pettigrew, J.D. (1995) Flying Primates: Crashed ? Or Crashed Through? Symp. zool. Soc. Lond. 67: pp 3-24.
This chapter summarises the evidence
for the flying primate hypothesis as it stood in 1993. It contains a number
of cladograms based upon the data of others showing good molecular support
from flying primates (e.g. lens alpha-crystallin, serum protein epitopes),
despite the overwhelming weight given to all the DNA sequencing studies
that appear to refute the hypothesis. As I have pointed, the DNA sequencing
studies are flawed by a large A+T bias. Recent DNA sequence studies have
appeared that fail to support bat monophyly, although it is still fair
to say that there is a general absence of support from DNA sequence data
for any special link between flying foxes and primates or flying foxes
and colugos. Such links are strongly predicted from other morphological
and molecular data, so their absence may be attributable to the extreme
modifications of the flying fox genome (A+T increase, genome size decrease).
16. Pettigrew, J.D. and Kirsch, J.A.W. (1997) The bat problem: I.
DNA-hybridisation melting curves based on DNA enriched for AT- or GC-content. Phil. Trans. Roy. Soc. B, 352: 1-12.
.
. Kirsch, J. A. W. & Pettigrew, J. D. (1997) Base compositional biases and the bat problem. II. DNA-hybridisation trees based on tracers enriched for AT- or GC- content. Phil. Trans. Roy. Soc. B, in press.
. Hutcheon, J.M., Kirsch, J.A.W., &Pettigrew, J.D. (1997) Base-compositional biases and the bat problem. III.the question of microchiropteran monophylyPhil. Trans. Roy. Soc. B, in press.
These papers all deal with the
possibility that a mutational bias, toward high A+T, has obscured the relationships
of the bats. The first paper shows that distances measured between flying
foxes and microbats, using DNA-DNA hybridisation techniques, are severely
underestimated because of the shared AT bias. The magnitude of the underestimate
is proportional to the degree of AT bias in the microbat member of the
pair, since AT bias varies considerably in microbats. The second and third
papers show that DNA hybridisation leads to a pairing between rhinolophoid
microbats and flying foxes, to the exclusion of all other microbats. This
pairing is anomalous and incompatible with most phylogenies of bats that
have been put forward, but can be explained in terms of AT bias, since
rhinolophoids have the highest AT bias of any microbat group.
*flying foxes = Old World fruit bats = Sub-Order Megachiroptera = megachiropterans = megabats = flughundes
?microbats = insectivorous bats
= Sub-Order Microchiroptera = micochiropterans = fledermaus