Flying primate hypothesis

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In evolutionary biology, the flying primate hypothesis is that megabats, a subgroup of Chiroptera (also known as flying foxes), form an evolutionary sister group of primates. The hypothesis began with Carl Linnaeus in 1758, and was again advanced by J.D. Smith in 1980. [1] It was proposed in its modern form by Australian neuroscientist Jack Pettigrew in 1986 [2] after he discovered that the connections between the retina and the superior colliculus (a region of the midbrain) in the megabat Pteropus were organized in the same way found in primates, and purportedly different from all other mammals. This was followed up by a longer study published in 1989, [3] in which this was supported by the analysis of many other brain and body characteristics. Pettigrew suggested that flying foxes, colugos, and primates were all descendants of the same group of early arboreal mammals. The megabat flight and the colugo gliding could be both seen as locomotory adaptations to a life high above the ground.

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The flying primate hypothesis met resistance from many zoologists. Its biggest challenges were not centered on the argument that megabats and primates are evolutionarily related, which reflects earlier ideas (such as the grouping of primates, tree shrews, colugos, and bats under the same taxonomic group, the Superorder Archonta). Rather, many biologists resisted the implication that megabats and microbats (or echolocating bats) formed distinct branches of mammalian evolution, with flight having evolved twice. This implication was borne out of the fact that microbats do not resemble primates in any of the neural characteristics studied by Pettigrew, instead resembling primitive mammals such as Insectivora in these respects. The advanced brain characters demonstrated in Pteropus could not, therefore, be generalized to imply that all bats are similar to primates.

More recently, the flying primate hypothesis was soundly rejected when scientists compared the DNA of bats to that of primates. These genetic studies support the monophyly of bats. [4] [5] [6] [7]

Neurological studies

Soon after Pettigrew's study, work on another genus of megabat ( Rousettus ) disputed the existence of an advanced pattern of connections between the retina and the superior colliculus. [8] However, this conclusion was later criticised on methodological grounds. [9] Later studies have sought further evidence of unique characteristics linking the megabat and primate brains. These studies have had limited success in identifying unique links between megabats and present-day primates, instead concluding that the megabat brain has characteristics that may resemble those likely to have existed in primitive primate brains. [10] Nonetheless, modern neuroanatomical studies have repeatedly supported the existence of very significant differences between the brains of megabats and microbats, which is one of the anchors of the "flying primate" hypothesis. [11] [12]

Biochemical studies

The implication that bats are diphyletic has been fiercely disputed by many zoologists, not only based on the unlikelihood that wings would have evolved twice in mammals, but also on biochemical studies of molecular evolution, which indicate that bats are monophyletic. [13] [14] However, other studies have disputed the validity of these conclusions. In particular, Pettigrew argued incorrectly that phylogenies based solely on DNA data can be subject to an artifact named the "base-compositional bias" [15] Further studies did not find base-compositional bias sufficient to discount support for the monophyly of bats. [16]

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References

  1. ↑ Pettigrew JD, Maseko BC, Manger PR (April 2008). "Primate-like retinotectal decussation in an echolocating megabat, Rousettus aegyptiacus". Neuroscience. 153 (1): 226–31. doi:10.1016/j.neuroscience.2008.02.019. PMID   18367343. S2CID   30649196.
  2. ↑ Pettigrew JD (1986). "Flying primates? Megabats have the advanced pathway from eye to midbrain". Science. 231 (4743): 1304–1346. Bibcode:1986Sci...231.1304P. doi:10.1126/science.3945827. PMID   3945827.
  3. ↑ Pettigrew JD, Jamieson BG, Robson SK, Hall LS, McAnally KI, Cooper HM (1989). "Phylogenetic relations between microbats, megabats and primates (Mammalia: Chiroptera and Primates)". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 325 (1229): 489–559. Bibcode:1989RSPTB.325..489P. doi:10.1098/rstb.1989.0102. PMID   2575767.
  4. ↑ Springer, Ms; Teeling, Ec; Madsen, O; Stanhope, Mj; De, Jong, Ww (May 2001). "Integrated fossil and molecular data reconstruct bat echolocation". Proceedings of the National Academy of Sciences of the United States of America. 98 (11): 6241–6. Bibcode:2001PNAS...98.6241S. doi: 10.1073/pnas.111551998 . PMC   33452 . PMID   11353869.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  5. ↑ Simmons, Nancy B.; Seymour, Kevin L.; Habersetzer, Jörg; Gunnell, Gregg F. (2008-02-14). "Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation" (PDF). Nature. 451 (7180): 818–821. Bibcode:2008Natur.451..818S. doi:10.1038/nature06549. hdl: 2027.42/62816 . PMID   18270539. S2CID   4356708.
  6. ↑ Teeling, Ec; Springer, Ms; Madsen, O; Bates, P; O'Brien, Sj; Murphy, Wj (January 2005). "A molecular phylogeny for bats illuminates biogeography and the fossil record". Science. 307 (5709): 580–4. Bibcode:2005Sci...307..580T. doi:10.1126/science.1105113. PMID   15681385. S2CID   25912333.
  7. ↑ Eick, Gn; Jacobs, Ds; Matthee, Ca (September 2005). "A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (chiroptera)" (Free full text). Molecular Biology and Evolution. 22 (9): 1869–86. doi: 10.1093/molbev/msi180 . PMID   15930153.
  8. ↑ Thiele A, Vogelsang M, Hoffmann KP (1991). "Pattern of retinotectal projection in the megachiropteran bat Rousettus aegyptiacus". Journal of Comparative Neurology. 314 (4): 671–683. doi:10.1002/cne.903140404. PMID   1816270. S2CID   2982155.
  9. ↑ Rosa MG, Schmid LM (1994). "Topography and extent of visual-field representation in the superior colliculus of the megachiropteran Pteropus". Visual Neuroscience. 11 (6): 1037–1057. doi:10.1017/S0952523800006878. PMID   7841115. S2CID   22400341.
  10. ↑ Ichida JM, Rosa MG, Casagrande VA (2000). "Does the visual system of the flying fox resemble that of primates? The distribution of calcium-binding proteins in the primary visual pathway of Pteropus poliocephalus". Journal of Comparative Neurology. 417 (1): 73–87. doi:10.1002/(SICI)1096-9861(20000131)417:1<73::AID-CNE6>3.0.CO;2-C. PMID   10660889. S2CID   7497545.
  11. ↑ Maseko BC, Manger PR (2007). "Distribution and morphology of cholinergic, catecholaminergic and serotonergic neurons in the brain of Schreiber's long-fingered bat, Miniopterus schreibersii". Journal of Chemical Neuroanatomy. 34 (3–4): 80–94. doi:10.1016/j.jchemneu.2007.05.004. PMID   17560075. S2CID   36492899.
  12. ↑ Maseko BC, Bourne JA, Manger PR (2007). "Distribution and morphology of cholinergic, putative catecholaminergic and serotonergic neurons in the brain of the Egyptian rousette flying fox, Rousettus aegyptiacus". Journal of Chemical Neuroanatomy. 34 (3–4): 108–127. doi:10.1016/j.jchemneu.2007.05.006. PMID   17624722. S2CID   21606575.
  13. ↑ Mindell DP, Dick CW, Baker RJ (1991). "Phylogenetic relationships among megabats, microbats, and primates". Proceedings of the National Academy of Sciences of the USA. 88 (22): 10322–10326. Bibcode:1991PNAS...8810322M. doi: 10.1073/pnas.88.22.10322 . PMC   52920 . PMID   1658803.
  14. ↑ Stanhope MJ, Czelusniak J, Si JS, Nickerson J, Goodman M (1992). "A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein, with convincing evidence for bat monophyly". Molecular Phylogenetics and Evolution. 1 (2): 148–60. doi:10.1016/1055-7903(92)90026-D. PMID   1342928.
  15. ↑ Hutcheon JM, Kirsch JA, Pettigrew JD (1998). "Base-compositional biases and the bat problem. III. The questions of microchiropteran monophyly". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 353 (1368): 607–617. doi:10.1098/rstb.1998.0229. PMC   1692242 . PMID   9602535.
  16. ↑ Van Den Bussche, R.A.; Baker, R.J.; Huelsenbeck, J.P.; Hillis, D.M. (1998). "Base compositional bias and phylogenetic analyses: a test of the "flying DNA" hypothesis". Mol Phylogenet Evol. 10 (3): 408–16. CiteSeerX   10.1.1.579.4292 . doi:10.1006/mpev.1998.0531. PMID   10051393.
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