Internal brooding favours pre-metamorphic chimerism in a non-colonial cnidarian, the sea anemone Urticina felina

Abstract

The concept of intraorganismal genetic heterogeneity resulting from allogeneic fusion (i.e. chimerism) has almost exclusively been explored in modular organisms that have the capacity to reproduce asexually, such as colonial ascidians and corals. Apart from medical conditions in mammals, the natural development of chimeras across ontogenetic stages has not been investigated in any unitary organism incapable of asexual propagation. Furthermore, chimerism was mainly studied among gregarious settlers to show that clustering of genetically similar individuals upon settlement promotes the occurrence of multi-chimeras exhibiting greater fitness. The possible occurrence of chimeric embryos and larvae prior to settlement has not received any attention. Here we document for the first time the presence of natural chimeras in brooded embryos and larvae of a unitary cnidarian, the sea anemone Urticina felina. Rates of visible bi-and multi-chimerism of up to 3.13 per cent were measured in the broods of 16 females. Apart from these sectorial chimeras, monitored fusion events also yielded homogeneous chimeric entities (mega-larvae) suggesting that the actual rates of natural chimerism in U. felina are greater than predicted by visual assessment. In support of this assumption, the broods of certain individuals comprised a dominant proportion (to 90%) of inexplicably large embryos and larvae (relative to oocyte size). Findings of fusion and chimerism in a unitary organism add a novel dimension to the framework within which the mechanisms and evolutionary significance of genetic heterogeneity in animal taxa can be explored.

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

“…Conflict arises primarily when larviparity (the release of offspring at the larval stage) is referred to as brooding (e.g., Siebert & Spaulding ; Mercier et al. ). The definition proposed here differs only slightly from Dunn's () definition: “the retention of offspring by a parent through the embryonic stages usually passed in the plankton, thereby shortening or entirely eliminating the dispersal stage” (p. 199).…”

“…Offspring of U. felina are known for chimerism via the fusing of two or more offspring (Mercier et al. ). The release of fused larvae may result in multiple settled and metamorphosed polyps joined together by tissues (morphological aberrants) or of single (homogenous) polyps composed of multiple larval sources (Mercier et al.…”

Complex offspring size effects: variations across life stages and between species

“…Although larval size in U. felina does not reflect initial egg provisioning due to fusion among siblings (Mercier et al. ; Sun et al. ), the total lipid content per larva ( μ g ind −1 ) followed the predicted increase with size.…”

“…Urticina felina larvae > 0.6 mm 2 (coined mega‐larvae) were shown to be formed by fusion of sibling embryos (Mercier et al. ; Sun et al. ).…”

The fester locus in Botryllus schlosseri experiences selection

“…Effective allorecognition systems are critical to the survival of organisms: the SI loci prevent inbreeding depression, T-lymphocytes educated by MHC molecules protect vertebrates against pathogens, and fusing to a closely related individual can provide competitive and reproductive advantages where space is limited and reproductive output is based on the size of the organism [1]. Allorecognition occurs across the tree of life [1], in anemones [2], angiosperms [3], ascidians [4-6], bacteria [7], bryozoans [8], cellular slime molds [9], corals [10], fungi [11], hydroids [12], gymnosperms [13,14], plasmodial slime molds [15], red algae [16], sponges [17], and vertebrates [18]. …”