Independent evolution of matrotrophy in the major classes of Bryozoa: transitions among reproductive patterns and their ecological background

Abstract

Bryozoa are unique among invertebrates in possessing placenta-like analogues and exhibiting extraembryonic nutrition in all high-level (class) taxa. Extant representatives of the classes Stenolaemata and Phylactolaemata are evidently all placental. Within the Gymnolaemata, placentalike systems have been known since the 1910s in a few species, but are herein reported to be widespread within this class. Placental forms include both viviparous species, in which embryonic development occurs within the maternal body cavity, and brooding species, in which development proceeds outside the body cavity. We have also identified an unknown reproductive pattern involving macrolecithal oogenesis and placental nutrition from a new, taxonomically extensive anatomical study of 120 species in 92 genera and 48 families of the gymnolaemate order Cheilostomata. Results support the hypothesis of evolution of oogenesis and placentation among Cheilostomata from oligolecithal to macrolecithal oogenesis, followed by brooding, through incipient matrotrophy combining macrolecithal oogenesis and placentation, to oligolecithal oogenesis with subsequent placental brooding. The distribution of reproductive patterns within the phylum suggests that variations of placentation evolved in all 3 bryozoan classes, and possibly several times within both gymnolaemate orders. We infer that extraembryonic nutrition may be advantageous to species through enhanced developmental plasticity, and, in fast-growing ephemeral colonies, simultaneous volumetric growth and embryonic development may facilitate earlier larval release and occupation of vacant space. KEY WORDS: Matrotrophy · Placenta · Reproductive patterns · Evolution · BryozoaResale or republication not permitted without written consent of the publisher

Pattern of occurrence of supraneural coelomopores and intertentacular organs in Gymnolaemata (Bryozoa) and its evolutionary implications

“…It should also be noted that in contrast with the hypothesis of Silén (1945), our scenario requires fewer evolutionary steps and corresponds to accepted ideas on the evolution of bryozoan sexual reproduction (Boardman et al 1983;Taylor 1988;Reed 1991;Taylor 2004, 2005;Ostrovsky et al 2009;Ostrovsky 2009). …”

“…However, the enlargement of the oocytes during the transition to the lecithotrophic larva in brooders (see Taylor 1988;Ostrovsky et al 2009) could make oviposition via the SNP more effective, and the ITO might be lost. On the other hand, the large oocyte size is obviously not an obstacle in some instances, since large oocytes are very elastic in gymnolaemate bryozoans.…”

Division of labor and recurrent evolution of polymorphisms in a group of colonial animals

“…This phylum is unique among invertebrates in that extraembryonic nutrition occurs in all major classes (Ostrovsky et al 2008(Ostrovsky et al , 2009a. Extraembryonic nutrition exists in at least 35 gymnolaemate (cheilostome plus ctenostome) genera among 26 families, and data from Harmer (1926), Cook (1985), and Kuklinski and Taylor (2006) suggest that there are likely to be more examples.…”

Do Gravid Females Become Selfish? Female Allocation of Energy during Gestation

“…Several studies have suggested that high maternal energy availability during gestation allows females to invest more energy in embryonic development. Such energy allocation is regarded as a selective advantage of matrotrophic reproduction (Trexler and DeAngelis 2003;Marsh-Matthews and Deaton 2006;Ostrovsky et al 2009;Itonaga et al 2012). If this is so, the relationship between food availability and the energetic costs of self-maintenance (i.e., net energy availability) during gestation may play a key role in the evolution of matrotrophic reproduction.…”