Abstract

During embryogenesis, organisms with lecithotrophic indirect development usually accumulate large quantities of energetic reserves in the form of yolk that are necessary for larval survival. Since all sponges have lecithotrophic development, yolk formation is an ineludible step of their embryogenesis. Sponge yolk platelets have a wide range of morphological forms, from entirely lipid or protein platelets to a combined platelet showing both lipids and proteins and even glycogen. So far, there are no comparative studies on the nature and content of yolk in congeneric species of sponges inhabiting contrasting environments, which could have putative effects on the larval adaptation to environmental conditions. Here, we have taken advantage of the worldwide distribution of the sponge genus Mycale, in order to compare the embryogenesis and yolk formation in two species inhabiting contrasting latitudinal areas: M. acerata from Antarctic waters and M. laevis from the Caribbean. We have compared their brooded embryos and larvae using scanning and transmission electron microscopy, and calculated their energetic signatures based on the nature of their yolk. While the general morphological feature of embryos and larvae of both species were very similar, the main difference resided in the yolk nature. The Antarctic species, M. acerata, showed exclusively lipid yolk, whereas the Caribbean species, M. laevis, showed combined platelets of lipids and proteins and less frequently protein yolk platelets. The larvae of M. acerata were estimated to possess a two-fold energetic signature compared to that of M. laevis, which may have important ecological implications for their survival and for maintaining large population densities in the cold waters of the Southern Ocean.

Highlights

  • Embryogenesis in sponges is a highly diverse process that can occur in the water column in oviparous species or within the sponge body in viviparous species, PLOS ONE | DOI:10.1371/journal.pone.0118805 March 18, 2015Comparative Ultrastructure of the Embryo in the Genus Mycale where it has more frequently been described [4]

  • Comparative morphology of reproductive elements in Mycale species. Both Mycale acerata and M. laevis are brooding species, with several embryonic stages within the same individual, which concurs with the observations in other Mycale species [38, 47]

  • The embryos of M. acerata and M. laevis were highly similar in size and shape, being strongly similar to the embryos and larvae of other

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Summary

Introduction

Embryogenesis in sponges is a highly diverse process that can occur in the water column in oviparous species or within the sponge body in viviparous species (see reviews by [1, 2, 3, 4]), PLOS ONE | DOI:10.1371/journal.pone.0118805 March 18, 2015Comparative Ultrastructure of the Embryo in the Genus Mycale where it has more frequently been described [4]. Embryogenesis in sponges is a highly diverse process that can occur in the water column in oviparous species or within the sponge body in viviparous species (see reviews by [1, 2, 3, 4]), PLOS ONE | DOI:10.1371/journal.pone.0118805. Several different morphogenetic movements often considered as a primitive form of gastrulation can occur, including delamination, invagination, and unipolar and multipolar egression (see [3] for a review). One of the most important processes during sponge embryogenesis is vitellogenesis, since all sponge larvae are lecithotrophic [5]. Yolk usually comprises several different cellular inclusions with either protein or lipid nature [6, 7]. Some sponges show homogenous yolk of either protein or lipid nature (e.g., [9, 17, 18, 19, 20, 21])

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