Bat Development

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Introduction

Short-tailed fruit bat Carollia perspicillata (embryonic stage 19)[1]

The bat (chiroptera) family consists of about 1,000 species throughout the world today (90 in Australia) and is not a common model of mammalian embryonic development.

The taxon chiroptera can also be further divided into the Megachiroptera (flying foxes) and Microchiroptera suborders. Echolocation sounds have been shown to differ in Microchiroptera (vocal cords) and Megachiroptera (tongue clicks).


Links: Stage 19 Quicktime Movie | Stage 19 Flash Movie | Hendra Virus | Category:Bat

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Some Recent Findings

  • Ovulation, fertilization, and early embryonic development in the menstruating fruit bat, Carollia perspicillata[2] "Graafian follicles developed large antra and exhibited preovulatory expansion of the cumulus oophorus. Ovulation had occurred in some on the morning, and in most by the evening, of day 1. The single ovum was released as a secondary oocyte and fertilized in the oviductal ampulla. Ovulated secondary oocytes were loosely associated with their cumulus cells, which were lost around the initiation of fertilization. Supernumerary spermatozoa were occasionally noted attached to the zonae pellucidae of oviductal ova, but never within the perivitelline space. By day 2, most ova had reached the pronuclear stage and by day 3, early cleavage stages. Several lines of evidence indicate that C. perspicillata is a spontaneous ovulator with a functional luteal phase."
  • Contrasting genetic structure in two co-distributed species of old world fruit bat [3] "The fulvous fruit bat (Rousettus leschenaulti) and the greater short-nosed fruit bat (Cynopterus sphinx) are two abundant and widely co-distributed Old World fruit bats in Southeast and East Asia. "
  • Digital gene expression tag profiling of bat digits provides robust candidates contributing to wing formation [4] "As the only truly flying mammals, bats use their unique wing - consisting of four elongated digits (digits II-V) connected by membranes - to power their flight. In addition to the elongated digits II-V, the forelimb contains one shorter digit (digit I) that is morphologically similar to the hindlimb digits. Here, we capitalized on the morphological variation among the bat forelimb digits to investigate the molecular mechanisms underlying digit elongation and wing formation."

Taxon

Chiroptera

Genbank common name: bats

Taxonomy Id: 9397 Rank: order

Genetic code: Translation table 1 (Standard)

Mitochondrial genetic code: Translation table 2 (Vertebrate Mitochondrial)

Lineage( abbreviated ): Eukaryota; Fungi/Metazoa group; Metazoa; Eumetazoa; Bilateria; Coelomata; Deuterostomia; Chordata; Craniata; Vertebrata; Gnathostomata; Teleostomi; Euteleostomi; Sarcopterygii; Tetrapoda; Amniota; Mammalia; Theria; Eutheria; Laurasiatheria

<qt>file=Bat embryo stage 19.mov‎|width=201px|height=220px|controller=true|autoplay=true</qt>

Species Comparison

Carollia perspicillata

  • (short-tailed fruit bat) Ovulation has a 24 hour variation with up to 2 days of variation in oviduct transit time, and gestation period is 113 - 120 days.

Myotis thysanodes and M. lucifugus

  • Ovulation, fertilization, and implantation occur during the first 2 weeks of May and gestation is 50 - 60 days for both species.

Embryonic Stages - Carollia perspicillata

Embryonic Bat Stages Carollia perspicillata[1]

Stage

Key features

Somites

Age
(dpc)

Uterus diameter
(mm)

Crown-rump length
(mm)

Mass
(mg)

12

Forelimb buds form; tail bud forms; caudal neuropore closes; 3 pharyngeal arches.

21-29

40

5.75
(+/- 0.64)

3.4
(+/- 0.42)

4.3
(+/- 1.7)

14

Retinal pigment; nasal pits; end of somitogenesis; propatagium and plagiopatagium primordia; hindlimb AER.

36-40

44

6.95
(+/- 0.44)

5.35
(+/- 0.24)

24.6
(+/- 3.6)

15

Hand plate and footplate form; lens vesicle; auditory hillocks; premaxillary centers.

46

8.65
(+/- 1.20)

7.45
(+/- 0.92)

56
(+/- 13)

16

Nose-leaf primordium; pinna and tragus form; forelimb digital condensations, uropatagium primordium.

50

12.06
(+/- 1.45)

8.66
(+/- 1.05)

110
(+/- 30)

17

Tongue protruding; cervical flexure straightens; hindlimb interdigit tissue receding; eyes begin to close.

54

13.45
(+/- 1.34)

9.15
(+/- 1.34)

114
(+/- 45)

18

Free thumb; head and body smoother, rounder; eyes half-closed; postaxial flexure at wrist; calcar.

60

16.32
(+/- 0.98)

12.35
(+/- 1.16)

278
(+/- 83)

20

Distal forelimbs overlap over face; head larger; eyelids cover pigmented retina; claw primordia form.

70

20.0
(+/- 3.54)

16.35
(+/- 1.06)

617
(+/- 156)

22

Prominent, triangular nose-leaf; eyelids reopening; wing membranes corrugated; claws pigmented, hooked.

80

23.03
(+/- 2.68)

20.02
(+/- 0.26)

1527
(+/- 208)

24

Fetal period commences; eyes completely open; face and nose-leaf pigmenting.

90

23.53
(+/- 0.64)

21.13
(+/- 0.06)

2097
(+/- 199)


(Values are mean n= 2-6, +/- standard deviation, original table contains more detailed data)

Thanks to Prof Richard Behringer and Dr Chris J. Creteko Dept. of Molecular Genetics, University of Texas M. D. Anderson Cancer Center, who provided images and stage information on the embryonic development of the Carollia perspicillata bat.

Embryonic Stages - Miniopterus schreibersii fuliginosus

Limb Development

Bat - adult and fetal limbs.jpg

Bat - adult and fetal limbs[4]

A - Left limbs of adult Myotis ricketti. DI, DII, DIII, DIV and DV represent digits I-V of the forelimb

B, C - Left limbs of Miniopterus schreibersii fuliginosus in the Fetal Stage as an example of samples used for the Myotis ricketti libraries. Libraries Hand DI and Hand DII-V are constructed from forelimb digit I and digits II-V, respectively. Library Foot is constructed from hindlimb digits I-V.

Bar = 1 cm in A; bar = 1 mm in B and C.

Neural Development

Bat - neural development 01.jpg

The short-tailed fruit bat Carollia perspicillata Stage 14 embryo nervous system as identified by neurofilament antibody (brown) staining. Neurofilament is an intermediate filament protein, forming part of the neuronal cytoskeleton.

Historic Images

Abnormalities

Rabies Virus

Rabies is a fatal encephalitis that can infect humans and is caused by lyssaviruses. Lyssavirus circulation has emerged in Southeast Asian bats.[5]


Links: Viral Infection - Lassa Virus

Hendra Virus

  • Hendra virus is a paramyxoviridae (ssRNA negative-strand virus) that mainly infects large fruit bats (flying foxes) which can be passed on to horses. * The infection has occasionally been passed onto people who have been in close contact with an infected horse.
  • There is evidence of fetal and placental infection in flying fox[6] and animal models.[7]
  • There is currently insufficient information to determine whether there are developmental effects in humans.
Links: NSW Public Health Sheet 2011 | Viralzone - Paramyxoviridae | Genome

References

  1. 1.0 1.1 Chris J Cretekos, Scott D Weatherbee, Chih-Hsin Chen, Nilima K Badwaik, Lee Niswander, Richard R Behringer, John J Rasweiler Embryonic staging system for the short-tailed fruit bat, Carollia perspicillata, a model organism for the mammalian order Chiroptera, based upon timed pregnancies in captive-bred animals. Dev. Dyn.: 2005, 233(3);721-38 PubMed 15861401
  2. John J Rasweiler, Nilima K Badwaik, Kiranmayi V Mechineni Ovulation, fertilization, and early embryonic development in the menstruating fruit bat, Carollia perspicillata. Anat Rec (Hoboken): 2011, 294(3);506-19 PubMed 21337714
  3. Jinping Chen, Stephen J Rossiter, Jonathan R Flanders, Yanhong Sun, Panyu Hua, Cassandra Miller-Butterworth, Xusheng Liu, Koilmani E Rajan, Shuyi Zhang Contrasting genetic structure in two co-distributed species of old world fruit bat. PLoS ONE: 2010, 5(11);e13903 PubMed 21085717
  4. 4.0 4.1 Zhe Wang, Dong Dong, Binghua Ru, Rebecca L Young, Naijian Han, Tingting Guo, Shuyi Zhang Digital gene expression tag profiling of bat digits provides robust candidates contributing to wing formation. BMC Genomics: 2010, 11;619 PubMed 21054883
  5. Kis Robertson, Boonlert Lumlertdacha, Richard Franka, Brett Petersen, Saithip Bhengsri, Sununta Henchaichon, Leonard F Peruski, Henry C Baggett, Susan A Maloney, Charles E Rupprecht Rabies-related knowledge and practices among persons at risk of bat exposures in Thailand. PLoS Negl Trop Dis: 2011, 5(6);e1054 PubMed 21738801 | PLoS Negl Trop Dis.
  6. Raina K Plowright, Hume E Field, Craig Smith, Anja Divljan, Carol Palmer, Gary Tabor, Peter Daszak, Janet E Foley Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc. Biol. Sci.: 2008, 275(1636);861-9 PubMed 18198149
  7. M M Williamson, P T Hooper, P W Selleck, H A Westbury, R F Slocombe Experimental hendra virus infectionin pregnant guinea-pigs and fruit Bats (Pteropus poliocephalus). J. Comp. Pathol.: 2000, 122(2-3);201-7 PubMed 10684689

Reviews

Rick A Adams Morphogenesis in bat wings: linking development, evolution and ecology. Cells Tissues Organs (Print): 2008, 187(1);13-23 PubMed 18163246

K E Sears Molecular determinants of bat wing development. Cells Tissues Organs (Print): 2008, 187(1);6-12 PubMed 18160799

R T Bernard, G S Cumming African bats: evolution of reproductive patterns and delays. Q Rev Biol: 1997, 72(3);253-74 PubMed 9293029

J J Rasweiler Pregnancy in chiroptera. J. Exp. Zool.: 1993, 266(6);495-513 PubMed 8371094


Articles

Chih-Hsin Chen, Chris J Cretekos, John J Rasweiler, Richard R Behringer Hoxd13 expression in the developing limbs of the short-tailed fruit bat, Carollia perspicillata. Evol. Dev.: 2005, 7(2);130-41 PubMed 15733311

J J Rasweiler, N K Badwaik Improved procedures for maintaining and breeding the short-tailed fruit bat (Carollia perspicillata) in a laboratory setting. Lab. Anim.: 1996, 30(2);171-81 PubMed 8783180


Search Pubmed: bat development | chiroptera development

External Links

External Links Notice - The dynamic nature of the internet may mean that some of these listed links may no longer function. If the link no longer works search the web with the link text or name.

Megabat | Molecular Phylogeny of Bats in Disarray


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Cite this page: Hill, M.A. (2015) Embryology Bat Development. Retrieved August 30, 2015, from https://embryology.med.unsw.edu.au/embryology/index.php/Bat_Development

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© Dr Mark Hill 2015, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G