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Molluscs represent a third phylum in which highly complex eyes are present. Cephalopod molluscs (squid, octopus, cuttlefish) possess a well developed nervous system and are highly intelligent (17). The complex eyes of cephalopod molluscs and vertebrates have been considered a classical example of convergent evolution (18). The eyes in these two systematic groups are remarkably similar in general appearance and organization but they are formed by different mechanisms during development and differ in many details.
(A) Nucleotide and deduced amino acid sequences of the squid L. opalescens embryonic Pax-6 cDNA. The paired domain and homeodomain are boxed. Two arrows indicate the positions of two known introns in the L. opalescens Pax-6 gene. (B) Comparison of the amino acid sequences between paired-, homeo- and C-terminal domains of vertebrate and invertebrate species. The squid sequence is shown in full; for other sequences only differing amino acids are shown. A - indicates gaps that were introduced to maximize similarities in the C-terminal domain; an * marks the end of the known nemertine sequence. The percent identities are shown for the squid sequence.
It is not clear at present whether squid Pax-6 initiates the development of ectopic eyes in Drosophila directly or indirectly by activating eyeless. Moreover, it is not known how many common genes acting downstream of Pax-6 are involved in the cascade leading to eye development in different systematic groups. At least two other candidate genes have been identified. One is eyes absent which is necessary for Drosophila eye development (51); two homologous genes for eyes absent are expressed in vertebrate lens and retina (52), and one homolog was recently identified in the squid (S.I.T., unpublished data). The homeobox gene, sine oculis, is also essential for eye development in Drosophila (53) and acts after eyes absent (54). The sine oculis homolog, Six-3, is expressed in the vertebrate eye (55). sine oculis homologs have not been identified yet in the squid.
We thank Dr. J. Marthy for help with the isolation of squid spermatophores for DNA isolation and Drs. W. Gilly and M. Perri for help with collection and fixing of squid embryos. We thank Drs. W. Gilly, P. Grant, and J. West for help with analysis of the results of in situ hybridization; A. Cvekl for pointing out the potential Pax-6 binding sites in S-crystallin promoters, and Frederick Biomedical Supercomputing Center, Frederick Cancer Research and Development Center (Frederick, MD) for allocation of computing time and staff support. This work has been supported by grants from the Swiss National Science Foundation and the Kantons of Basel To W.G., from the Janggen-Pöhn Stiftung to G.H., and from the Collen Foundation and the Sandoz Foundation to P.C.
A staging series based on easily distinguishable morphological features is a basic and necessary tool for developmental studies. It provides a consistent reference for comparisons between independent studies, negates the need to know when fertilization occurred, allows correlation of the phase of development with the time of development (to facilitate collection of embryos at specific stages), and allows comparisons between species. Given the growing interest in Hawaiian bobtail squid (Euprymna scolopes) as a contemporary cephalopod developmental system, this article provides a detailed survey of E. scolopes embryogenesis from cleavage through hatching under controlled environmental conditions, including detailed descriptions of externally visible morphological features that are easily distinguished in either live or freshly fixed embryos under a dissecting microscope. Photomicrographs are also provided to aid in the accurate and rapid staging of E. scolopes embryos.
Developmental biology is among the many subdisciplines of the life sciences being transformed by our increasing awareness of the role of coevolved microbial symbionts in health and disease.