TY - JOUR

T1 - Independent evolution of matrotrophy in the major classes of Bryozoa

T2 - Transitions among reproductive patterns and their ecological background

AU - Ostrovsky, Andrew N.

AU - Gordon, Dennis P.

AU - Lidgard, Scott

PY - 2009

Y1 - 2009

N2 - 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, placenta-like systems have been known since the 1910s in a few species, but are herein reported to be wide-spread 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.

AB - 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, placenta-like systems have been known since the 1910s in a few species, but are herein reported to be wide-spread 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.

KW - Bryozoa

KW - Evolution

KW - Matrotrophy

KW - Placenta

KW - Reproductive patterns

UR - http://www.scopus.com/inward/record.url?scp=63649153485&partnerID=8YFLogxK

U2 - 10.3354/meps07850

DO - 10.3354/meps07850

M3 - Article

VL - 378

SP - 113

EP - 124

JO - Marine Ecology - Progress Series

JF - Marine Ecology - Progress Series

SN - 0171-8630

ER -