Repeated evolution of eye loss in Mexican cavefish: Evidence of similar developmental mechanisms in independently evolved populations.

Evolution in similar environments often leads to convergence of behavioral and anatomical traits. A classic example of convergent trait evolution is the reduced traits that characterize many cave animals: reduction or loss of pigmentation and eyes. While these traits have evolved many times, relatively little is known about whether these traits repeatedly evolve through the same or different molecular and developmental mechanisms. The small freshwater fish, Astyanax mexicanus, provides an opportunity to investigate the repeated evolution of cave traits. A. mexicanus exists as two forms, a sighted, surface-dwelling form and at least 29 populations of a blind, cave-dwelling form that initially develops eyes that subsequently degenerate. We compared eye morphology and the expression of eye regulatory genes in developing surface fish and two independently evolved cavefish populations, Pachón and Molino. We found that many of the previously described molecular and morphological alterations that occur during eye development in Pachón cavefish are also found in Molino cavefish. However, for many of these traits, the Molino cavefish have a less severe phenotype than Pachón cavefish. Further, cave-cave hybrid fish have larger eyes and lenses during early development compared with fish from either parental population, suggesting that some different changes underlie eye loss in these two populations. Together, these data support the hypothesis that these two cavefish populations evolved eye loss independently, yet through some of the same developmental and molecular mechanisms.

Parallel evolution of regressive and constructive craniofacial traits across distinct populations of Astyanax mexicanus cavefish.

Life in complete darkness has driven the evolution of a suite of troglobitic features in the blind Mexican cavefish Astyanax mexicanus, such as eye and pigmentation loss. While regressive evolution is a hallmark of obligate cave-dwelling organisms, constructive (or augmented) traits commonly arise as well. The cavefish cranium has undergone extensive changes compared with closely-related surface fish. These alterations are rooted in both cranial bones and surrounding sensory tissues such as enhancements in the gustatory and lateral line systems. Cavefish also harbor numerous cranial bone asymmetries: fluctuating asymmetry of individual bones and directional asymmetry in a dorsal bend of the skull. This asymmetry is mirrored by the asymmetrical patterning of mechanosensory neuromasts. We explored the relationship between facial bones and neuromasts using in vivo fluorescent colabeling and microcomputed tomography. We found an increase in neuromast density within dermal bone boundaries across three distinct populations of cavefish compared to surface-dwelling fish. We also show that eye loss disrupts early neuromast patterning, which in turn impacts the development of dermal bones. While cavefish exhibit alterations in cranial bone and neuromast patterning, each population varied in the severity. This variation may reflect observed differences in behavior across populations. For instance, a bend in the dorsal region of the skull may expose neuromasts to water flow on the opposite side of the face, enhancing sensory input and spatial mapping in the dark.

Unilateral microphthalmia or anophthalmia in eight pythons (Pythonidae).

OBJECTIVE: To provide morphological descriptions of microphthalmia or anophthalmia in eight pythons using microcomputerized tomography (µCT), magnetic resonance imaging (MRI), and histopathology. ANIMALS STUDIED: Seven Burmese pythons (Python bivittatus) and one ball python (P. regius) with clinically normal right eyes and an abnormal or missing left eye. PROCEDURE: At the time of euthanasia, four of the eight snakes underwent necropsy. Hereafter, the heads of two Burmese pythons and one ball python were examined using µCT, and another Burmese python was subjected to MRI. Following these procedures, the heads of these four pythons along with the heads of an additional three Burmese pythons were prepared for histology. RESULTS: All eight snakes had left ocular openings seen as dermal invaginations between 0.2 and 2.0 mm in diameter. They also had varying degrees of malformations of the orbital bones and a limited presence of nervous, glandular, and muscle tissue in the posterior orbit. Two individuals had small but identifiable eyes. Furthermore, remnants of the pigmented embryonic framework of the hyaloid vessels were found in the anophthalmic snakes. Necropsies revealed no other macroscopic anomalies. CONCLUSIONS: Eight pythons with unilateral left-sided microphthalmia or anophthalmia had one normal eye and a left orbit with malformed or incompletely developed ocular structures along with remnants of fetal structures. These cases lend further information to a condition that is often seen in snakes, but infrequently described.

Congenital ocular and adnexal disorders in reptiles.

Ocular and adnexal congenital disorders are those that manifest at birth and could involve single or multiple tissues. Several abnormalities have been reported in literature affecting reptilian ocular and/or adnexal tissues. The objectives of this review are: (i) review those disorders previously reported in reptile literature; (ii) present new cases; (iii) provide a basic classification of them according to the moment of occurrence and (iv) indirectly, encourage the clinician dealing with these cases to go further in their diagnosis. The authors consider that categorizing ocular and adnexal congenital disorders could help the clinician to deal with them. The categorization of these disorders required an intense review of cases previously reported in literature and allows the authors suspect that some of them could not have been accurately diagnosed according to the definitions of the anomalies and/or not accurately described. The authors consider that ocular and adnexal congenital disorders could have been underestimated in reptiles and further studies could be helpful to promote the description of new disorders and to expand the knowledge about those previously reported. The review will first describe abnormalities reported during organogenesis (describing possible etiopathogenesis, cases reported, an approach to their diagnosis and recommended therapeutic options).Then a mention of the ocular disorders occurring after organogenesis is made. These disorders are divided when possible in those affecting all or most part of the globe and those affecting only specific tissues (surface ectoderm, neurocrest and mesenchyma and neuroectoderm).

Growth and Behavior of Congenitally Anophthalmic Lee-Sung Pigs.

Circadian rhythm is usually regulated by the environmental light-dark cycle. Congenitally anophthalmic miniature pigs provide a valuable model for the study of factors affecting circadian rhythms in the absence of visual exposure to the light-dark cycle. This study investigated the growth and daily behavior patterns of Lee-Sung pigs with congenital anophthalmia. Growth in 5 Lee-Sung pigs (LSP) with congenital anophthalmia (LSP-A) and 10 normally developed pigs (LSP-N) was assessed when they were 1 through 6 mo old. Behavioral studies using digital video recording were completed in 6 sexually mature LSP (3 LSP-A and 3 LSP-N). MRI showed that LSP-A lose their vision because of a lack of retinal input and optic chiasm development. LSP-N and LSP-A did not differ in body weight or size at 2, 4, and 6 mo of age. Behavior and activity pattern studies showed that both LSP-A and LSP-N were active mainly during daylight, but LSP-A spent significantly more time exploring their environment during the day (28%) and night (10%) than did LSP-N. This study revealed that growth performance was similar between LSP-A and normal pigs, but their behavior and activity patterns differed. LSP-A showed circadian rhythm abnormalities similar to those in blind humans. This study provides basic data on LSP-A as a model for studying compensatory cross-modal brain plasticity and hormone regulation in the absence of retinal input is deficient and for understanding the role of circadian rhythm regulation.

Anophthalmia in a Wild Eastern Gray Squirrel (Sciurus carolinensis).

We describe bilateral true anophthalmia in a juvenile female eastern gray squirrel (Sciurus carolinensis) with histologic confirmation that orbital contents lacked ocular tissues. Additionally, the optic chiasm of the brain was absent and axon density in the optic tract adjacent to the lateral geniculate nucleus was reduced.

Thalamic afferents to the visual cortex in congenitally anophthalmic mice.

Retrograde cell labelling with horseradish peroxidase (HRP) has been used to study the thalamic afferents to the primary visual cortex (area 17) in mutant H1-ZRDCT-An ('eyeless') mice, in which the eyes are missing throughout development. Injections of HRP that were localised to a subregion of area 17, resulted in the labelling of a group of neurons in the ipsilateral dorsal lateral geniculate nucleus, showing the existence of a point-to-point connectivity. Many labelled cells were also found in other posterior thalamic nuclei especially in the lateral posterior nucleus which in normal animals contain very few or no labelled cells.

A behavioral profile of bilateral anophthalmic mutant rats.

A behavioral profile of hereditary bilateral anophthalmic mutant rat was studied in different light: dark schedules. The control and mutant rats were acclimatized to either a) a 12h light:12h dark cycle or b) continuous darkness or c) continuous illumination. The measurements of spontaneous motor activity with Opto Varimex and behavioral despair in a swim test were conducted. The daily food consumption and plasma glucose levels were also measured. The study indicated that, unlike the control rats, mutants did not exhibit any time dependent change in the spontaneous motor activity in any of the three different lighting conditions. A strong biphasic feeding burst was also not affected by anophthalmia in mutant rats. Our findings on spontaneous motor activity and the feeding pattern are contrary to those in the existing literature.

Unilateral anophthalmia in a Holstein calf.

Unilateral anophthalmia in a Holstein calf was examined morphologically. On the left side, a small cystic remnant of the eye ball (CRE) was present in the orbit. The CRE was adhered to the dura mater through an abnormal foramen formed in the orbital region of the cranial base. At this region of the left cerebral hemisphere, a porencephalic change was detected. Histologically, the pigment epithelium was continued from the lining of the inner surface of CRE to the residual cerebrocortical tissue attached to the dura mater. These characteristic changes seem to suggest the partial fusion of the outer layer of the optic cup to the telencephalon during optic organogenesis.

Congenital anophthalmia with caudal vertebral anomalies in Japanese Brown cattle.

Anophthalmia and caudal vertebral anomalies such as taillessness or wry tail were morphologically examined in ten Japanese Brown calves obtained in Kumamoto Prefecture. The anomalous calves lacked eyeball bilaterally or unilaterally but had small-sized eyelids and narrow palpebral fissures. A small cystic, solid or spot-like remnant of eyeball (REB) was buried in the mixture of vestigial extraocular muscles, lacrimal gland and adipose tissue of the orbit. The REB was composed of irregularly arranged elements of ocular wall such as sclera, choroid and retina. The retina was often dysplastic and connected to the hypoplastic optic nerve. These morphological changes might represent the defective processes after the formation of the optic vesicle or cup. Therefore, this eye defect may be defined as degenerative anophthalmia. The defects of the vertebral body such as wedge vertebra, hemivertebra, and sagittal cleft vertebra seen in the lumbar, sacral, and coccygial regions and the meandering of the axial line of abnormal vertebrae may suggest the failure of notochord formation in the early fetal period. From the embryological point of view, it seemed possible that the calves were exposed to teratogen at the critical time of optic organogenesis and notochordal formation. The cause of anomalies could not be determined in this study.

[Bilateral anophthalmia associated with further anomalies of the head in German Holstein calves]. / Bilaterale Anophthalmie in Verbindung mit weiteren Missbildungen im Kopfbereich bei Deutschen Holsteinkälbern.

Two female calves of the breed German Holsteins showing bilateral anophthalmia and deformations of the jaws such as brachygnathia superior and bilateral cleft of lips and noses, respectively, were born on two different farms. Similar congenital defects could be found neither in the relatives of the affected calves nor in other animals of the same herds. A monogenic autosomal recessive inheritance may have caused bilateral anophthalmia. Chromosomal aberrations could not be detected in the affected calves. The possible environmental causes such as infection by the BVD-virus or oversupply or deficiency of vitamin A are very unlikely.

The oculomotor nucleus and extraocular muscles in a mutant anophthalmic mouse.

The object of this study was to determine whether the oculomotor nucleus and the extraocular muscles are present in the adult of a mutant mouse strain in which eye formation fails early in development (Chase and Chase, '41). Neuronal counts for the oculomotor (IIIrd) nucleus were obtained from serial paraffin sections made through the midbrains of seven mice of the anophthalmic mutant group (ZRDCT-An) and seven mice of the same strain in which eyes were present (ZRDCT-N). The orbital structures of the anophthalmic and control groups were reconstructed from 1-micrometer plastic serial sections. There was in the anophthalmic mouse, in the same location as in the normal, an oculomotor nucleus whose mean neuronal cell number was 206 (+/- 40). The normal mouse had a mean value of 262 (+/- 63) oculomotor neurons. On the basis of these results, this difference between the two groups was not statistically significant (P = 0.073). The neuronal number per cubic millimeter was similar in the two groups (P = 0.81). In the orbit of the anophthalmic mouse, several bundles of striated muscle occupied a location comparable to that of extraocular muscle in the normal mouse. Neuromuscular junctions were present on fibers of this orbital muscle. It is concluded that the early failure of eye formation does not prevent the development of extraocular muscles and the oculomotor nucleus, and their retention in the adult.

Spontaneous malformations in squirrel monkey [Saimiri sciureus] fetuses with emphasis on cleft lip and palate.

Gross examination of a group of surviving and nonsurviving squirrel monkeys has revealed a high incidence of cleft lip and cleft primary palate defects with an associated anophthalmia. These defects, as well as single incidences of diaphragmatic aplasia, scoliosis, internal hydrocephalus, and funnel chest, are noted or described and discussed with reference to sex and parentage.

Anophthalmia and retinal degeneration associated with stenosis of the optic foramen in Fischer 344 rats.

Bilateral anophthalmia was discovered in a male rat (No. 1) and unilateral anophthalmia was found in the left eye of two female rats (Nos. 2 and 3) derived from a Fischer 344 inbred colony. One male rat (No. 4), a littermate of No. 3, had externally normal eyes, but his left eye had severe retinal atrophy, which was detected by ophthalmoscopy. The eyelids in both eyes of No. 1 and in the left eyes of Nos. 2 and 3 were present. Radiography of the skull revealed small optic foramina on both sides of No. 1 and on the affected side of Nos. 2, 3, and 4. Histologically, both globes and optic nerves (ONs) of No. 1 and the left globe and ONs of Nos. 2 and 3 were completely missing. Diffuse retinal degeneration in the left globe and axonal degeneration in the left ON and the right optic tract were observed in No. 4. Dysplasia of the sphenoid bone associated with stenosis of the optic foramen was detected on the affected side of all rats. Thus, ON aplasia in anophthalmic rats and atrophic ON in a rat with retinal degeneration seem to be closely related to stenosis of the optic foramen.

The primary ultrastructural defect caused by anophthalmic white (Wh) in the Syrian hamster.

Anophthalmic white (Wh) of the Syrian hamster is a highly pleiotropic dominant spotting color mutation causing homozygotes to be deaf, blind, and white. An ultrastructural analysis of embryonic tissue reveals that Wh causes the retention of cilia by cells of opposing layers of the embryonic retina and by the lens fiber cells. Previous ultrastructural analyses indicate that Wh also causes the retention of cilia by secretory cells of the anterior lobe of adult pituitaries. We propose that the primary ultrastructural defects caused by Wh is the retention of cilia by embryonic cells. These retained cilia are hypothesized to interfere with normal cell-cell interactions and subsequent cell differentiation.