Embryonic staging of bats with special reference to Vespertilio sinensis and its cochlear development.

BACKGROUND: How bats deviate heterochronically from other mammals remains largely unresolved, reflecting the lack of a quantitative staging framework allowing comparison among species. The standard event system (SES) is an embryonic staging system allowing quantitative detection of interspecific developmental variations. Here, the first SES-based staging system for bats, using Asian parti-colored bat (Vespertilio sinensis) is introduced. General aspects of normal embryonic development and the three-dimensional development of the bat cochlea were described for the first time. Recoding the embryonic staging tables of 18 previously reported bat species and Mus musculus into the SES system, quantitative developmental comparisons were performed. RESULTS: It was found that limb bud development of V. sinensis is relatively late among 19 bat species and late limb development is a shared trait of vespertilionid bats. The inner ear cochlear canal forms before the semicircular canal in V. sinensis while the cochlear canal forms after the semicircular canal in non-volant mammals. CONCLUSIONS: The present approach using the SES system provides a powerful framework to detect the peculiarities of bat development. Incorporating the timing of gene expression patterns into the SES framework will further contribute to the understanding of the evolution of specialized features in bats.

Postcranial heterochrony, modularity, integration and disparity in the prenatal ossification in bats (Chiroptera).

BACKGROUND: Self-powered flight is one of the most energy-intensive types of locomotion found in vertebrates. It is also associated with a range of extreme morpho-physiological adaptations that evolved independently in three different vertebrate groups. Considering that development acts as a bridge between the genotype and phenotype on which selection acts, studying the ossification of the postcranium can potentially illuminate our understanding of bat flight evolution. However, the ontogenetic basis of vertebrate flight remains largely understudied. Advances in quantitative analysis of sequence heterochrony and morphogenetic growth have created novel approaches to study the developmental basis of diversification and the evolvability of skeletal morphogenesis. Assessing the presence of ontogenetic disparity, integration and modularity from an evolutionary approach allows assessing whether flight may have resulted in evolutionary differences in the magnitude and mode of development in bats. RESULTS: We quantitatively compared the prenatal ossification of the postcranium (24 bones) between bats (14 species), non-volant mammals (11 species) and birds (14 species), combining for the first time prenatal sequence heterochrony and developmental growth data. Sequence heterochrony was found across groups, showing that bat postcranial development shares patterns found in other flying vertebrates but also those in non-volant mammals. In bats, modularity was found as an axial-appendicular partition, resembling a mammalian pattern of developmental modularity and suggesting flight did not repattern prenatal postcranial covariance in bats. CONCLUSIONS: Combining prenatal data from 14 bat species, this study represents the most comprehensive quantitative analysis of chiropteran ossification to date. Heterochrony between the wing and leg in bats could reflect functional needs of the newborn, rather than ecological aspects of the adult. Bats share similarities with birds in the development of structures involved in flight (i.e. handwing and sternum), suggesting that flight altriciality and early ossification of pedal phalanges and sternum are common across flying vertebrates. These results indicate that the developmental modularity found in bats facilitates intramodular phenotypic diversification of the skeleton. Integration and disparity increased across developmental time in bats. We also found a delay in the ossification of highly adaptable and evolvable regions (e.g. handwing and sternum) that are directly associated with flight performance.

Role of putrescine in ovary and embryo development in fruit bat Cynopterus sphinx during embryonic diapause.

The aim of this study was to evaluate the effect of putrescine on ovarian activity and the rate of embryonic development in Cynopterus sphinx during delayed development. The result showed the presence of a rate-limiting enzyme, ornithine decarboxylase-1, in both ovary and utero-embryonic unit of C. sphinx suggests a synthesis of putrescine in these sites. The corpus luteum showed increased, whereas utero-embryonic unit showed decreased production of putrescine during delayed development as compared with the normal development. The bat treated in vivo with putrescine during delayed development showed increase in progesterone and estradiol synthesis, correlated with increased expression of luteinizing hormone receptor, steroidogenic acute receptor protein, and 3ß-hydroxysteroid dehydrogenase through extracellular signal-regulated kinase (ERK1/2)-mediated pathway in the ovary; but showed increase in the weight and expression of progesterone receptor (PR), B-cell lymphoma 2, proliferating cell nucleus antigen, and vascular endothelial growth factor proteins in utero-embryonic unit. The in vitro treatment of putrescine showed stimulatory whereas treatment with an inhibitor of putrescine, 2-difluoromethylornithine caused an inhibitory effect on ovarian progesterone synthesis and cell proliferation, and cell survival in the utero-embryonic unit. In conclusion, the putrescine showed two separate roles during embryonic diapause, high concentration of putrescine in the ovary may support corpus luteum and basal synthesis of progesterone, whereas a low level of putrescine causes retarded embryonic development by inhibiting cell proliferation in the utero-embryonic unit. The bat treated with putrescine either directly promotes cell proliferation, cell survival, and angiogenic activities or acts indirectly increasing PR on utero-embryonic unit thereby activating development in delayed embryo in C. sphinx.

Adiposity associated changes in serum glucose and adiponectin levels modulate ovarian steroidogenesis during delayed embryonic development in the fruit bat, Cynopterus sphinx.

The aim of the present study was to evaluate the mechanism by which embryonic development in Cynopterus sphinx is impaired during the period of increased accumulation of white adipose tissue during winter scarcity of food. The change in the mass of white adipose tissue during adipogenesis showed significant positive correlation with the circulating glucose level. But increase in circulating glucose level during the adipogenesis showed negative correlation with circulating progesterone and adiponectin levels. The in vivo study showed increased glucose uptake by the adipose tissue during adipogenesis due to increased expression of insulin receptor (IR) and glucose transporter (GLUT) 4 proteins. This study showed decline in the adiponectin level during fat accumulation. In the in vitro study, ovary treated with high doses of glucose showed impaired progesterone synthesis. This is due to decreased glucose uptake mediated decrease in the expression of luteinizing hormone-receptor, steroidogenic acute regulatory protein, IR, GLUT4 and AdipoR1 proteins. But the ovary treated with adiponectin either alone or with higher concentration of glucose showed improvement in progesterone synthesis due to increased expression of IR, GLUT4 and AdipoR1 mediated increased glucose uptake. In conclusion, increased circulating glucose level prior to winter dormancy preferably transported to white adipose tissue for fat accumulation diverting glucose away from the ovary. Consequently the decreased availability of adiponectin and glucose to the ovary and utero-embryonic unit may be responsible for impaired progesterone synthesis and delayed embryonic development. The delayed embryonic development in Cynopterus sphinx may have evolved, in part, as a mechanism to prevent pregnancy loss during the period of decreased energy availability.

Prolactin modulates luteal activity in the short-nosed fruit bat, Cynopterus sphinx during delayed embryonic development.

The aim of this study was to evaluate the role of prolactin as a modulator of luteal steroidogenesis during the period of delayed embryonic development in Cynopterus sphinx. A marked decline in circulating prolactin levels was noted during the months of November through December coinciding with the period of decreased serum progesterone and delayed embryonic development. The seasonal changes in serum prolactin levels correlated positively with circulating progesterone (P) level, but inversely with circulating melatonin level during first pregnancy showing delayed development in Cynopterus sphinx. The results also showed decreased expression of prolactin receptor-short form (PRL-RS) both in the corpus luteum and in the utero-embryonic unit during the period of delayed embryonic development. Bats treated in vivo with prolactin during the period of delayed development showed significant increase in serum progesterone and estradiol levels together with significant increase in the expression of PRL-RS, luteinizing hormone receptor (LH-R), steroidogenic acute receptor protein (STAR) and 3ß-hydroxysteroid dehydrogenase (3ß-HSD) in the ovary. Prolactin stimulated ovarian angiogenesis (vascular endothelial growth factor) and cell survival (B-cell lymphoma 2) in vivo. Significant increases in ovarian progesterone production and the expression of prolactin-receptor, LH-R, STAR and 3ß-HSD proteins were noted following the exposure of LH or prolactin in vitro during the delayed period. In conclusion, short-day associated increased melatonin level may be responsible for decreased prolactin release during November-December. The decline in prolactin level might play a role in suppressing P and estradiol-17ß (E2) estradiol levels thereby causing delayed embryonic development in C. sphinx.

Patterns of postcranial ossification and sequence heterochrony in bats: life histories and developmental trade-offs.

The recently increased interest in studies on sequence heterochrony has uncovered developmental variation between species. However, how changes in developmental program are related to shifts in life-history parameters remains largely unsolved. Here we provide the most comprehensive data to date on postcranial ossification sequence of bats and compare them to various boreoeutherian mammals with different locomotive modes. Given that bats are equipped with an elongated manus, we expected to detect characteristic heterochronies particularly related to wing development. Although heterochronies related to wing development were confirmed as predicted, unexpected heterochronies regarding the pedal digits were also found. The timing of ossification onset of pedal phalanges is earlier than other mammals. Particularly, bats deviate from others in that pedal phalanges initiate ossification earlier than manual phalanges. It is known that the foot size of new born bats is close to that of adults, and that it takes several weeks to month until the wing is developed for flight. Given that the foot is required to be firm and stable enough at the time of birth to allow continued attachment to the mother and/or cave walls, we suggest that the accelerated development of the hind foot is linked to their unique life history. Since the forelimb is not mature enough for flight at birth and requires extended postnatal time to be large enough to be fully functional, we postulate that bats invest in earlier development of the hindlimb. We conclud that energy allocation trade-offs can play a significant role in shaping the evolution of development.

Role of adiponectin in delayed embryonic development of the short-nosed fruit bat, Cynopterus sphinx.

The aim of this study was to evaluate the role of adiponectin in the delayed embryonic development of Cynopterus sphinx. Adiponectin receptor (ADIPOR1) abundance was first observed to be lower during the delayed versus non-delayed periods of utero-embryonic unit development. The effects of adiponectin treatment on embryonic development were then evaluated during the period of delayed development. Exogenous treatment increased the in vivo rate of embryonic development, as indicated by an increase in weight, ADIPOR1 levels in the utero-embryonic unit, and histological changes in embryonic development. Treatment with adiponectin during embryonic diapause showed a significant increase in circulating progesterone and estradiol concentrations, and in production of their receptors in the utero-embryonic unit. The adiponectin-induced increase in estradiol synthesis was correlated with increased cell survival (BCL2 protein levels) and cell proliferation (PCNA protein levels) in the utero-embryonic unit, suggesting an indirect effect of adiponectin via estradiol synthesis by the ovary. An in vitro study further confirmed the in vivo findings that adiponectin treatment increases PCNA levels together with increased uptake of glucose by increasing the abundance of glucose transporter 8 (GLUT8) in the utero-embryonic unit. The in vitro study also revealed that adiponectin, together with estradiol but not alone, significantly increased ADIPOR1 protein levels. Thus, adiponectin works in concert with estradiol to increase glucose transport to the utero-embryonic unit and promote cell proliferation, which together accelerate embryonic development.

[Key morphofunctional transformations in the evolution of chiropterans (Bats, Chiroptera)].

Study on the morphology and morphogenesis of wing membranes in Bats has revealed some peculiarities in their structure and development. Understanding the embryogenesis of these animals, as well as attraction of data obtained on their molecular genetics and paleontology, allows one to single out some factors that could have initiated evolutionary modifications in development programs. A scenario of the key morphofunctional transformations in the forelimbs during the evolution of chiropterans is given.

Establishment of cell line from embryonic tissue of Pipistrellus ceylonicus bat species from India & its susceptibility to different viruses.

BACKGROUND & OBJECTIVES: Pipistrellus ceylonicus bat species is widely distributed in South Asia, with additional populations recorded in China and Southeast Asia. Bats are the natural reservoir hosts for a number of emerging zoonotic diseases. Attempts to isolate bat-borne viruses in various terrestrial mammalian cell lines have sometimes been unsuccessful. The bat cell lines are useful in isolation and propagation of many of the viruses harboured by bats. New stable bat cell lines are needed to help such investigations and to assist in the study of bat immunology and virus-host interactions. In this study we made an attempt to develop a cell line from P. ceylonicus bats. METHODS: An effort was made to establish cell line from embryo of P. ceylonicus species of bat after seeding to Dulbecco's modified eagle medium (DMEM) supplemented with 10 per cent foetal bovine serum; a primary cell line was established and designated as NIV-BtEPC. Mitochondrial DNA profile analysis was done using cyt-b and ND-1 gene sequences from the cell line. Phylogenetic tree was constructed using neighbour-joining algorithm for cyt-b and ND-1 genes with 1000-bootstrap replicates. RESULTS: NIV-BtEPC cell line was susceptible to Chandipura (CHPV) and novel adenovirus (BtAdv-RLM) isolated from Rousettus leschenaulti from India but did not support multiplication of a number of Bunyaviruses, Alphaviruses and Flavivirus. This might be useful for isolation of a range of viruses and investigation of unknown aetiological agents. INTERPRETATION & CONCLUSIONS: In this study, a new bat cell line was developed from P. ceylonicus. This cell line was successfully tested for the susceptibility to Chandipura and BtAdv-RLM virus isolated from bats. The approach developed and optimised in this study may be applicable to the other species of bats and this established cell line can be used to facilitate virus isolation and basic research into virus-host interaction.

Early oogenesis in the short-tailed fruit bat Carollia perspicillata: transient germ cell cysts and noncanonical intercellular bridges.

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.

Embryonic evidence uncovers convergent origins of laryngeal echolocation in bats.

Bats are the second-most speciose group of mammals, comprising 20% of species diversity today. Their global explosion, representing one of the greatest adaptive radiations in mammalian history, is largely attributed to their ability of laryngeal echolocation and powered flight, which enabled them to conquer the night sky, a vast and hitherto unoccupied ecological niche. While there is consensus that powered flight evolved only once in the lineage, whether laryngeal echolocation has a single origin in bats or evolved multiple times independently remains disputed. Here, we present developmental evidence in support of laryngeal echolocation having multiple origins in bats. This is consistent with a non-echolocating bat ancestor and independent gain of echolocation in Yinpterochiroptera and Yangochiroptera, as well as the gain of primitive echolocation in the bat ancestor, followed by convergent evolution of laryngeal echolocation in Yinpterochiroptera and Yangochiroptera, with loss of primitive echolocation in pteropodids. Our comparative embryological investigations found that there is no developmental difference in the hearing apparatus between non-laryngeal echolocating bats (pteropodids) and terrestrial non-bat mammals. In contrast, the echolocation system is developed heterotopically and heterochronically in the two phylogenetically distant laryngeal echolocating bats (rhinolophoids and yangochiropterans), providing the first embryological evidence that the echolocation system evolved independently in these bats.

A comparative study of prenatal development in Miniopterus schreibersii fuliginosus, Hipposideros armiger and H. pratti.

BACKGROUND: Bats comprise the second largest order of mammals. However, there are far fewer morphological studies of post-implantation embryonic development than early embryonic development in bats. RESULTS: We studied three species of bats (Miniopterus schreibersii fuliginosus, Hipposideros armiger and H. pratti), representing the two suborders Yangochiroptera and Yinpterochiroptera. Using an established embryonic staging system, we identified the embryonic stages for M. schreibersii fuliginosus, H. armiger and H. pratti and described the morphological changes in each species, including the development of the complex and distinctive nose-leaves in H. armiger and H. pratti. Finally, we compared embryonic and fetal morphology of the three species in the present study with five other species for which information is available. CONCLUSION: As a whole, the organogenetic sequence of bat embryos is uniform and the embryos appear homoplastic before Stage 16. Morphological differentiation between species occurs mainly after embryonic Stage 16. Our study provides three new bat species for interspecific comparison of post-implantation embryonic development within the order Chiroptera and detailed data on the development of nose-leaves for bats in the superfamily Rhinolophoidea.

Melatonin regulates delayed embryonic development in the short-nosed fruit bat, Cynopterus sphinx.

The aim of the present study was to evaluate the seasonal variation in serum melatonin levels and their relationship to the changes in the serum progesterone level, ovarian steroidogenesis, and embryonic development during two successive pregnancies of Cynopterus sphinx. Circulating melatonin concentrations showed two peaks; one coincided with the period of low progesterone synthesis and delayed embryonic development, whereas the second peak coincided with regressing corpus luteum. This finding suggests that increased serum melatonin level during November-December may be responsible for delayed embryonic development by suppressing progesterone synthesis. The study showed increased melatonin receptors (MTNR1A and MTNR1B) in the corpus luteum and in the utero-embryonic unit during the period of delayed embryonic development. The in vitro study showed that a high dose of melatonin suppressed progesterone synthesis, whereas a lower dose of melatonin increased progesterone synthesis by the ovary. The effects of melatonin on ovarian steroidogenesis are mediated through changes in the expression of peripheral-type benzodiazepine receptor, P450 side chain cleavage enzyme, and LH receptor proteins. This study further showed a suppressive impact of melatonin on the progesterone receptor (PGR) in the utero-embryonic unit; this effect might contribute to delayed embryonic development in C. sphinx. The results of the present study thus suggest that a high circulating melatonin level has a dual contribution in retarding embryonic development in C. sphinx by impairing progesterone synthesis as well as by inhibiting progesterone action by reducing expression of PGR in the utero-embryonic unit.

Artibeus jamaicensis: delayed embryonic development in a neotropical bat.

In Panama the phyllostomid bat Artibeus jamaicensis is seasonally polyestrous, and young are born in March or April and July or August. Blastocysts conceived after the second birth implant in the uterus but are dormant from September to mid-November, when normal development again resumes.

Luteal cell steroidogenesis in relation to delayed embryonic development in the Indian short-nosed fruit bat, Cynopterus sphinx.

The primary aim of this study was to determine the possible cause of slow or delayed embryonic development in Cynopterus sphinx by investigating morphological and steroidogenic changes in the corpus luteum (CL) and circulating hormone concentrations during two pregnancies of a year. This species showed delayed post-implantational embryonic development during gastrulation of the first pregnancy. Morphological features of the CL showed normal luteinization during both pregnancies. The CL did not change significantly in luteal cell size during the delay period of the first pregnancy as compared with the second pregnancy. The circulating progesterone and 17beta-estradiol concentrations were significantly lower during the period of delayed embryonic development as compared with the same stage of embryonic development during the second pregnancy. We also showed a marked decline in the activity of 3beta-hydroxysteroid dehydrogenase, P450 side chain cleavage enzyme, and steroidogenic acute regulatory peptide in the CL during the delay period. This may cause low circulating progesterone and estradiol synthesis and consequently delay embryonic development. What causes the decrease in steroidogenic factors in the CL during the period of delayed development in C. sphinx is under investigation.

Normal embryonic development of the greater horseshoe bat Rhinolophus ferrumequinum, with special reference to nose leaf formation.

The order Chiroptera (bats) is the second largest group of mammals, composed of more than 1,300 species. Although powered flight and echolocation in bats have attracted many biologists, diversity in bat facial morphology has been almost neglected. Some bat species have a "nose leaf," a leaf-like epithelial appendage around their nostrils. The nose leaf appears to have been acquired at least three times independently in bat evolution, and its morphology is highly diverse among bats species. Internal tissue morphology of nose-leaves has been investigated through histological analyses of late-stage fetuses of some bat species possessing the nose leaf. However, the proximate factors that bring about chiropteran nose-leaves have not been identified. As an initial step to address the question above, we describe the normal embryonic development of the greater horseshoe bat Rhinolophus ferrumequinum, and examine development of the tissues associated with their nose leaf during embryogenesis through histological analyses. We found that the nose leaf of R. ferrumequinum is formed through two phases. First, the primordium of the nose leaf appears as two tissue bulges aligned top and bottom on the face at embryonic stages 15-16. Second, the sub-regions of the nose leaf are differentiated through ingrowth as well as outgrowth of the epithelium at stage 17. In embryogenesis of Carollia perspicillata, a phyllostomid species with a nose leaf, the nose leaf primordium is formed as a small tissue bulge on the nostril at stage 17. This tissue bulge grows into a dorsally projected thin epithelial structure. Such differences in the nose leaf developmental process between chiropteran lineages may suggest that distinct developmental mechanisms have been employed in each lineage's nose leaf evolution.

An examination of the Chiropteran HoxD locus from an evolutionary perspective.

Duplications of Hox gene clusters have been suggested as a mechanism whereby new Hox functions can be developed while preserving critical ancestral roles. However, in tetrapods, particularly in mammals, there is great variability in limb structure morphologies that are known to be affected by Hox genes without further Hox cluster duplications. The lack of further duplications suggests that if Hox genes have played a direct role in the morphological elaboration of tetrapod limbs, the changes must have come about from Hox protein sequence changes or from changes regarding the amount, time, and place of Hox gene expression. To investigate whether such changes to Hox genes could play a role in limb elaboration, we examined the HoxD locus in bats, which have both highly elaborated fore- and hindlimbs. We found that while the Chiropteran HoxD13 protein was highly conserved, there was an expansion of HoxD13 expression in the posterior portion of the Chiropteran forelimb and into the leading edge of the wing membrane. We were also able to uncover a number of unique lineage-specific sequence changes to a known HoxD limb enhancer, the Global Control Region (GCR). Further, mouse transgenic assays showed that the Chiropteran GCR has new limb enhancer activity domains beyond that reported for the Human GCR. These results suggest that modulation of Hox gene expression may be a mechanism for effecting morphological change in lineage-specific manner while maintaining ancestral constraints and cluster integrity.

Growth and development of two species of bats in a shared maternity roost.

Skeletogenesis was studied in two species of bats, Myotis austroriparius (southeastern brown bat) and Tadarida brasiliensis (Brazilian free-tailed bat), occupying a maternity roost in central Florida. These bats often use distinct maternity roost environments, so this provided an opportunity to examine differential patterns of long bone growth while fetuses and newborn developed under similar environmental conditions. Some differences in the timing of onset of osteogenesis were revealed in the bats, indicating that some elements of the hindlimb develop relatively more rapidly in T. brasiliensis than in M. austroriparius. Some variance was also noted, with similarity to other species previously studied by others, in the exact timing and elongation of both long bones, as well as carpal and tarsal bones. In contrast to many elements of the long appendicular skeleton of developing Mus musculus, the bats all exhibit relatively precocial patterns of osteogenesis during which cartilaginous precursors are replaced by bone tissue. The relative advanced timing of osteogenesis in select hindlimb bones of T. brasiliensis may account for its relatively low neonatal mortality compared to M. austroriparius newborn in the same roost.

Forelimb versus hindlimb skeletal development in the big brown bat, Eptesicus fuscus: functional divergence is reflected in chondrocytic performance in Autopodial growth plates.

The morphology of the chiropteran forelimb demonstrates musculoskeletal specializations for powered flight essentially unique among mammals, including extreme elongation of the distal skeletal elements. Recent studies have focused primarily on the relative timing and levels of gene expression during early stages of endochondral ossification in the chiropteran embryo for clues to the molecular basis of the evolutionary origins of flight in these species. The goal of the current study was to examine how elongation of skeletal elements of the forelimb autopod is achieved through a combination of cellular proliferation, cellular enlargement and matrix synthesis during a period of rapid postnatal growth in Eptesicus fuscus. Quantitative analyses were done of multiple performance parameters of growth plate chondrocytes during all phases of the differentiation cascade. Fourteen autopodial growth plates from the forelimb and hindlimb of one individual, as well as the proximal tibial growth plate, were collected and analyzed. Significant differences were seen in all performance parameters examined. Particularly striking were the differences between growth plates of the manus and pes in the size of the pool of chondrocytes in all cellular zones and rates of turnover of terminal cells. The magnitude of hypertrophy of chondrocytes in growth plates of the manus in E. fuscus far exceeded what has been reported previously in any species, even in rapidly elongating rodent long bones. Volume changes approaching x70 and height changes of 50-60 mum/cell (paralleling the direction of growth) occurred after proliferation in the most rapidly growing growth plates. The data demonstrate that final differences in lengths of homologous skeletal elements in the autopod of the forelimb and hindlimb of this species result not just from an initiating factor early in development, but from continued quantitative differences in chondrocytic performance during postnatal bone elongation as measured by multiple kinetic-based parameters.

Morphogenesis in bat wings: linking development, evolution and ecology.

The evolution of powered flight in mammals required specific developmental shifts from an ancestral limb morphology to one adapted for flight. Through studies of comparative morphogenesis, investigators have quantified points and rates of divergence providing important insights into how wings evolved in mammals. Herein I compare growth,development and skeletogenesis of forelimbs between bats and the more ancestral state provided by the rat (Rattus norvegicus)and quantify growth trajectories that illustrate morphological divergence both developmentally and evolutionarily. In addition, I discuss how wing shape is controlled during morphogenesis by applying multivariate analyses of wing bones and wing membranes and discuss how flight dynamics are stabilized during flight ontogeny. Further, I discuss the development of flight in bats in relation to the ontogenetic niche and how juveniles effect populational foraging patterns. In addition, I provide a hypothetical ontogenetic landscape model that predicts how and when selection is most intense during juvenile morphogenesis and test this model with data from a population of the little brown bat, Myotis lucifugus.