TRAIT LOSS AND THE EVOLUTION OF BIODIVERSITY

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Trait loss is an important driver of organismal diversity (O’Malley et al., 2016). Across animal lineages there are numerous examples of speciation events associated with gene/genome loss (e.g., among obligate parasites), organ/tissue loss (e.g., eyeless cave fishes), and even the loss of multicellularity (e.g., yeast).  Ctenophores (comb jellies) provide an unparalleled opportunity to study both the origin of a novel cell type (the ctenophore-specific colloblast) and the mechanisms responsible for its loss. Found exclusively in the tentacles, colloblasts are specialized secretory cells that release an adhesive secretion used to capture passing prey. This unusual cell type is an ancestral character of Ctenophora; yet, one lineage of ctenophores (genus Beroe + genus Haeckelia) has lost their colloblasts entirely, feeding only on other ctenophores (genus Beroe) or cnidarians (genus Haeckelia). We take advantage of this natural variation in distantly related ctenophores to study the factors that promote the evolution of morphological diversity. 

Previous studies have mapped the fate of each embryonic micromere (up to the 32-cell stage) in the colloblast-rich ctenophore Mnemiopsis leidyi (Martindale and Henry, 1997,1999). From this, we know that micromeres in the "e" lineage make a significant contribution of the development of the tentacle apparatus. Ctenophores in the genus Beroe do not make tentacles or colloblasts at any stage of development and the fate of their "e" micromeres is currently unknown. By comparing embryonic development in M. leidyi and Beroe ovata we aim to understand the evolutionary diversification of cell identity in a single cell lineage. If "e" micromeres no longer make colloblasts in Beroe, what do they make...? And how?

Loss of cells/structures need not be associated with loss of genes. Indeed, reduced selection pressure can release genes from the burden of maintaining established connections in the ancestral gene regulatory network (GRN) and permit the evolution of novel binding sites and/or novel activation domains. Relaxed selection on the GRN controlling colloblast specification in Beroe may have allowed genes formerly restricted to colloblasts to acquire new functions. Using RNAseq in Mnemiopsis leidyi, we previously identified nearly 200 colloblast-specific genes (Babonis et al., 2018) providing the first molecular characterization of this novel (and truly bizarre) cell type. By investigating the function of colloblast-specific genes in Beroe ovata, we aim to characterize the fate of genes that no longer encode colloblast identity.

Babonis, L.S., DeBiasse, M.B., Francis, W.R., Christianson, L.M., Moss, A.G., Haddock, S.H.D., Martindale, M.Q., Ryan, J.F., 2018. Integrating embryonic development and evolutionary history to characterize tentacle-specific cell types in a ctenophore. Mol Biol Evol 35, 2940-2956 Link

Martindale, M.Q., Henry, J.J., 1997. Experimental analysis of tentacle formation in the Ctenophore Mnemiopsis leidyi. Biol Bull-Us 193, 245-247 Link

Martindale, M.Q., Henry, J.Q., 1999. Intracellular fate mapping in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages. Developmental biology 214, 243-257 Link

O’Malley, M.A., Wideman, J.G., Ruiz-Trillo, I., 2016. Losing complexity: The role of simplification in macroevolution. Trends Ecol Evol 31, 608-621 Link