Remarkable Shifts in Offspring Provisioning during Gestation in a Live-Bearing Cnidarian

Abstract

Animals display diverse means of producing and provisioning offspring, from eggs to embryos and juveniles. While external development predominates, many forms of embryonic incubation have evolved, including placentation in mammals and a number of understudied variants in basal metazoans that could help understand evolutionary diversification. Here we studied the brooding sea anemone Aulactinia stella, using behavioural, morphological and biochemical indicators of offspring phenotype to characterize gestation and elucidate parental and sibling relationships. The pronounced variance in juvenile weight within broods was not strongly related to any of the typical external predictors (adult weight, clutch size, sampling date, environmental conditions). Lipid concentration was significantly higher in the tissues of the small juveniles than in those of large juveniles or adult, and fatty acid profiles tended to set small juveniles apart. Finally, intra-brood feeding on external resources was documented in larger juveniles. These results are consistent with ontogenetic shifts in nutrition, from vitellogenic provisioning to post-zygotic nourishment to a prenatal form of nursing upon acquisition of feeding organs, highlighting matrotrophic and conflict-driven mechanisms acting on offspring phenotype during gestation.

Brooding sea anemones (Cnidaria: Anthozoa: Actiniaria): paragons of diversity in mode, morphology, and maternity

“…Evidence in support of Verrill's () suggestion that internally brooded offspring derive nutriment from the adult has been recently corroborated in accounts of matrotrophy (extra‐vitellogenic nourishment) in Aulactinia stella by Mercier et al. ().…”

“…In addition, actiniarians can use dissolved organic matter (Shick 1991) as a source of nutrition and this may be important for any juveniles bathed in seawater but not exposed to significant sources of prey. Evidence in support of Verrill's (1869) suggestion that internally brooded offspring derive nutriment from the adult has been recently corroborated in accounts of matrotrophy (extravitellogenic nourishment) in Aulactinia stella by Mercier et al (2016).…”

“…There is some evidence that larger internally brooded offspring feed directly on food items ingested by the parent (Chia & Rostron ; Mercier et al. ). Internally brooded 12‐ and 24‐tentacle‐stage individuals of Phymanthus crucifer were capable of feeding on Artemia in the laboratory immediately upon removal from the parent (Jennison ).…”

<p class="HeadingRunIn"><strong>Arrangement and size variation of intra-gonadal offspring in a viviparous asterinid sea star</strong></p>

“…For species that care for their young internally, offspring interact with the parent and may compete with siblings for limited resources; these interactions may influence size variation at birth (Schrader & Travis 2009;Kamel et al 2010B). Parent-offspring conflict and sibling competition are more intense in species that provide extra-embryonic nutrition, a mode of parental care called matrotrophy (Frick 1998;Schrader & Travis 2009;Mercier et al 2016;Ostrovsky et al 2015;Kamel & Williams 2017). Extreme sibling competition may result in cannibalism where the progeny ingest eggs (oophagy) or siblings (embryophagy/adelphophagy) (Lesoway et al 2014;Ostrovsky et al 2015).…”