Selected Publications

Page, L.R. 2000. Development and evolution of adult feeding structures in caenogastropods: overcoming larval functional constraints. Evolution & Development 2: 25-34.

Page, L.R. and Pedersen, R.V.K. 1998. Transformation of phytoplanktivorous larvae into predatory carnivores during the development of Polinices lewisii (Mollusca, Caenogastropoda). Invertebrate Biology 117: 208-220.

These papers address an important question in the sphere of evolutionary developmental biology.  How can specialized adult structures evolve from larval precursors when larval functional requirements impose potential constraints to radical change in form?  The system we examined is particularly significant because the complex foregut of predatory gastropods has been called a key evolutionary innovation, which facilitated a dramatic adaptive radiation among late Mesozoic and early Cenozoic gastropods. Polinices [Euspira] lewisii and Nassarius mendicus transform from pelagic, microalgae-feeding larvae to predatory carnivores within 3 days of metamorphic induction.  Analysis of the process revealed that this drastic and rapid change in food type and feeding method is facilitated by a dramatic developmental novelty.  The adult buccal mass is formed from a semi-isolated oupocketing of the larval foregut.  At metamorphosis, the distal larval foregut is destroyed and the pre-formed post-metamorphic buccal mass is put in place in a process that involves de novo formation of the definitive mouth.
 
 

The image on the left is a metamorphically competent larva of the moon snail Polinices [Euspira] lewisii. The image on the right is a scanning electron micrograph of a bivalved ostracod exoskeleton that has been drilled by a young juvenile of P. lewisii. Young juveniles of this snail also feed on newly recruited bivalve molluscs.

Data obtained from scanning and transmission electron microscopy and from immunohistochemical techniques for detecting serotonin-like antigenicity were used to characterize the larval apical ganglion in four species of caenogastropods.  Our observations, when combined with those of earlier studies, suggest that common ancestry is a major determinant of overall structural design for the apical ganglion in caenogastropods and heterobranchs, which are sister groups within the Gastropoda. Velum size and life history strategy may account for some, but not all, cases of interspecific differences in the serotonergic component of this component of the larval nervous system.
 

The scanning electron micrographs on the left show the site (large arrow in A) where sensory dendrites of the apical ganglion penetrate the cephalic epidermis of a larva of Euspira lewisii. SH = larval shell; T = cephalic tentacles; VL = velar lobes. The image in B shows this area at higher magnification; arrows indicate two tufts of cilia.
The micrographs on the right were obtained with a scanning laser confocal microscope and show serotonin immunoreactive neurons and neurites within the apical ganglion of Trichotropis cancellata (upper image) and Amphissa versicolor (lower image).

Shell-attached retractor muscles of gastropods are of prime importance to existing theories about early gastropod evolution.  Results of this paper, when combined with results of two earlier papers on larval gastropod shell muscles (collectively providing comparative data for three major gastropod clades), point to a highly conserved pattern for muscle morphogenesis that may be a fundamental component of the developing gastropod Baupln.  An immediate consequence of this paper is the undermining of a widely accepted theory that invokes heterochrony for the evolutionary emergence of caenogastropods from an archaeogastropod-like ancestor.  Comparative studies of the developing shell muscles of gastropods is an ongoing project in my lab, which may provide insight into the nature of the developmental modifications that generated gastropod torsion.
 

Computer-assisted reconstructions of retractor muscles in sectioned larvae of Polinices lewisii at two stages of development. Blue = muscle; red = nervous system; green = distal foregut.  One profile of the velar lobes is shown in brown.
· The image on the left shows the trunk and several distal fibre tracts of the larval retractor muscle (lrm) in a hatching larva reconstructed in dorsal view.  The asterisk indicates the site where the muscle is anchored on the larval shell (shell is not reconstructed).
· The image on the right shows the pedal tract of the post-metamorphic columellar muscle, which has differentiated in this 25 day old larva of Polinices.  The asterisk indicates the position of the columella of the shell.  Contrary to earlier opinion about the developmental origins of the caenogastropod columellar muscle, the columellar muscle of Polinices is a different muscle than the larval retractor muscle that was present in newly hatched larvae.

Page, L.R. 1997. Larval shell muscles in the abalone Haliotiskamtschatkana.
Biological Bulletin 193: 30-46.
 

An early description of Haliotis (abalone) development has had a major impact on current theories about the evolutionary emergence of gastropod molluscs, but the results have never been verified using modern, high resolution methods. I used ultrastructural techniques to examine the development of the mantle cavity and shell attached retractor muscles in a species of Haliotis.  My analysis uncovered inaccuracies in the previous description and the revised information forces a reconsideration of long-standing theories about gastropod torsion.
 
 

Scanning electron micrograph of the calcified shell of H. kamtschatkana at approximately one week after metamorphosis.