Early oogenesis in the short-tailed fruit bat Carollia perspicillata: transient germ cell cysts and noncanonical intercellular bridges
Genesis. 2012 Jan;50(1):18-27. doi: 10.1002/dvg.20780. Epub 2011 Aug 23.
Lechowska A1, Bilinski SM, Rasweiler JJ 4th, Cretekos CJ, Behringer RR, Kloc M.
The ovaries of early embryos (40 days post coitum/p.c.) of the bat Carollia perspicillata contain numerous germ-line cysts, which are composed of 10 to 12 sister germ cells (cystocytes). Variability in the number of cystocytes within the cyst and between the cysts (defying the Giardina rule) indicates that the mitotic divisions of the cystoblast are asynchronous in this bat species. Serial section analysis showed that the cystocytes are interconnected via intercellular bridges that are atypical, strongly elongated, short-lived, and rich in microtubule bundles and microfilaments. During slightly later stages of embryonic development (44-46 days p.c.), somatic cells penetrate the cyst, and their cytoplasmic projections separate individual oocytes. Separated oocytes surrounded by a single layer of somatic cells constitute the primordial ovarian follicles. The oocytes of C. perspicillata are similar to mouse oocytes and are asymmetric. In both species, this asymmetry is clearly recognizable in the localization of the Golgi complexes. The presence of germ-line cysts and intercellular bridges (although noncanonical) in the fetal ovaries of C. perspicillata suggest that the formation of germ-line cysts is an evolutionarily conserved phase in the development of the female gametes in a substantial part of the animal kingdom. Copyright © 2011 Wiley Periodicals, Inc. PMID 21681920
Is tissue maturation necessary for flight? Changes in body composition during postnatal development in the big brown bat
J Comp Physiol B. 2011 Apr;181(3):423-35. Epub 2010 Nov 3.
Hood WR, Oftedal OT, Kunz TH. Source Center for Ecology and Conservation Biology, Department of Biology, Boston University, Boston, MA 02215, USA. firstname.lastname@example.org
Patterns of offspring development reflect the availability of energy and nutrients, limitations on an individual's capacity to use available resources, and tradeoffs between the use of nutrients to support current metabolic demands and tissue growth. To determine if the long period of offspring dependency in bats is associated with the need for an advanced state of tissue maturation prior to flight, we examined body composition during postnatal growth in the big brown bat, Eptesicus fuscus. Despite their large size at birth (22% of maternal mass), newborn bats are relatively immature, containing 82% body water in fat-free mass. However, the total body water content of newborn bat pups decreases to near-adult levels in advance of weaning, while concentrations of total body fat and protein exceed adult values. In contrast to many other mammals, postnatal growth of bat pups was characterized by relatively stable concentrations of calcium and phosphorus, but declining concentrations of magnesium. These levels remained stable or rebounded in late postnatal development. This casts doubt on the hypothesis that low rates of mineral transfer necessitate an extended lactation period in bats. However, our finding of near-adult body composition at weaning is consistent with the hypothesis that extended lactation in bats is necessary for the young to achieve sufficient tissue maturity to undertake the active flight necessary for independent feeding. In this respect, bats differ from most other mammals but resemble birds that must engage in active flight to achieve nutritional independence.
Postnatal development in Andersen's leaf-nosed bat Hipposideros pomona: flight, wing shape, and wing bone lengths
Zoology (Jena). 2011 Apr;114(2):69-77.
Lin AQ, Jin LR, Shi LM, Sun KP, Berquist SW, Liu Y, Feng J.
Source Jilin Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, 5268 Renmin Road, Changchun 130024, China.
Postnatal changes in flight development, wing shape and wing bone lengths of 56 marked neonate Hipposideros pomona were investigated under natural conditions in southwest China. Flight experiments showed that pups began to flutter with a short horizontal displacement at 10 days and first took flight at 19 days, with most achieving sustained flight at 1 month old. Analysis of covariance on wingspan, wing area, and the other seven wing characteristics between 'pre-flight' and 'post-volancy' periods supports the hypothesis that growth had one 'pre-flight' trajectory and a different 'post-volancy' trajectory in bats. Wingspan, handwing length and area, armwing length and area, and total wing area increased linearly until the age of first flight, after which the growth rates decreased (all P < 0.001). Wing loading declined linearly until day 19 before ultimately decreasing to adult levels (P < 0.001). Additionally, the relationship of different pairwise combinations of bony components composing span-wise length and chord-wise length was evaluated to test the hypothesis that compensatory growth of wing bones in H. pomona occurred in both 'pre-flight' and 'post-volancy' periods. The frequency of short-long and long-short pairs was significantly greater than that of short-short, long-long pairs in most pairs of bone elements in adults. The results indicate that a bone 'shorter than expected' would be compensated by a bone or bones 'longer than expected', suggesting compensatory growth in H. pomona. The pairwise comparisons conducted in adults were also performed in young bats during 'pre-flight' and 'post-volancy' periods, demonstrating that compensatory growth occurred throughout postnatal ontogeny.
Copyright © 2011 Elsevier GmbH. All rights reserved.
Ovulation, fertilization, and early embryonic development in the menstruating fruit bat, Carollia perspicillata
Anat Rec (Hoboken). 2011 Mar;294(3):506-19. doi: 10.1002/ar.21304. Epub 2010 Dec 2.
Rasweiler JJ 4th, Badwaik NK, Mechineni KV.
Department of Obstetrics and Gynecology, State University of New York Downstate Medical Center, 450 Clarkson Avenue, Brooklyn, NY 11203, USA. email@example.com
To characterize periovulatory events, reproductive tracts were collected at 12 hr intervals from captive-bred, short-tailed fruit bats, Carollia perspicillata, on days 1-3 post coitum and examined histologically. Most bats bred readily. 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. Most newly mated females had recently formed, but regressing corpora lutea, and thickened (albeit menstrual) uteri despite having been housed with males only for brief periods (<23 days). Menstruation is usually periovulatory in this species. Furthermore, the interval between successive estrus periods in most mated females that failed to establish ongoing pregnancies at the first was 21-27 days. Menstruation involved substantial endometrial desquamation, plus associated bleeding, and generally extended to the evening of day 3, the last time point studied. In nearly all females with a recent corpus luteum (n = 24 of 25; 96%), the preovulatory or newly ruptured follicle was in the opposite ovary.
Copyright © 2010 Wiley-Liss, Inc.
Contrasting genetic structure in two co-distributed species of old world fruit bat
PLoS One. 2010 Nov 10;5(11):e13903.
Chen J, Rossiter SJ, Flanders JR, Sun Y, Hua P, Miller-Butterworth C, Liu X, Rajan KE, Zhang S. Source Guangdong Entomological Institute, Guangzhou, China.
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. The former species forms large colonies in caves while the latter roots in small groups in trees. To test whether these differences in social organization and roosting ecology are associated with contrasting patterns of gene flow, we used mtDNA and nuclear loci to characterize population genetic subdivision and phylogeographic histories in both species sampled from China, Vietnam and India. Our analyses from R. leschenaulti using both types of marker revealed little evidence of genetic structure across the study region. On the other hand, C. sphinx showed significant genetic mtDNA differentiation between the samples from India compared with China and Vietnam, as well as greater structuring of microsatellite genotypes within China. Demographic analyses indicated signatures of past rapid population expansion in both taxa, with more recent demographic growth in C. sphinx. Therefore, the relative genetic homogeneity in R. leschenaulti is unlikely to reflect past events. Instead we suggest that the absence of substructure in R. leschenaulti is a consequence of higher levels of gene flow among colonies, and that greater vagility in this species is an adaptation associated with cave roosting.
Digital gene expression tag profiling of bat digits provides robust candidates contributing to wing formation
BMC Genomics. 2010 Nov 6;11:619.
Wang Z, Dong D, Ru B, Young RL, Han N, Guo T, Zhang S. Source Institute of Molecular Ecology and Evolution, iAIR, East China Normal University, Shanghai 200062, PR China.
BACKGROUND: 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. Using next generation sequencing technology, we performed digital gene expression tag profiling (DGE-tag profiling) of developing digits in a pooled sample of two Myotis ricketti and validated our sequencing results using real-time quantitative PCR (RT-qPCR) of gene expression in the developing digits of two Hipposideros armiger.
RESULTS: Among hundreds of genes exhibiting significant differences in expression between the short and long digits, we highlight 14 genes most related to digit elongation. These genes include two Tbx genes (Tbx3 and Tbx15), five BMP pathway genes (Bmp3, RGMB, Smad1, Smad4 and Nog), four Homeobox genes (Hoxd8, Hoxd9, Hoxa1 and Satb1), and three other genes (Twist1, Tmeff2 and Enpp2) related to digit malformations or cell proliferation. In addition, our results suggest that Tbx4 and Pitx2 contribute to the morphological similarity and five genes (Acta1, Tnnc2, Atp2a1, Hrc and Myoz1) contribute to the functional similarity between the thumb and hindlimb digits.
CONCLUSIONS: Results of this study not only implicate many developmental genes as robust candidates underlying digit elongation and wing formation in bats, but also provide a better understanding of the genes involved in autopodial development in general.
A comparative study of prenatal development in Miniopterus schreibersii fuliginosus, Hipposideros armiger and H. pratti
Wang Z, Han N, Racey PA, Ru B, He G. BMC Dev Biol. 2010 Jan 21;10:10.
PMID 20092640 PMC: 2824742
The role of early development in mammalian limb diversification: a descriptive comparison of early limb development between the Natal long-fingered bat (Miniopterus natalensis) and the mouse (Mus musculus)
Dev Dyn. 2009 Apr;238(4):965-79.
Hockman D, Mason MK, Jacobs DS, Illing N. Source Department of Molecular and Cell Biology, University of Cape Town, Cape Town, South Africa.
Comparative embryology expands our understanding of unique limb structures, such as that found in bats. Bat forelimb digits 2 to 5 are differentially elongated and joined by webbing, while the hindlimb digits are of similar length in many species. We compare limb development between the mouse and the Natal long-fingered bat, Miniopterus natalensis, to pinpoint the stage at which their limbs begin to differ. The bat forelimb differs from the mouse at Carollia stage (CS) 14 with the appearance of the wing membrane primordia. This difference is enhanced at CS 15 with the posterior expansion of the hand plate. The bat hindlimb begins to differ from the mouse between CS 15 and 16 when the foot plate undergoes a proximal expansion resulting in digit primordia of very similar length. Our findings support recent gene expression studies, which reveal a role for early patterning in the development of the bat limb. Copyright 2009 Wiley-Liss, Inc.