Kin Discrimination in Protists: From Many Cells to Single Cells and Backwards

Abstract

During four decades (1960s to 1990s), the conceptualization and experimental design of studies in kin recognition relied on work with multicellular eukaryotes, particularly Unikonta (including invertebrates and vertebrates) and some Bikonta (including plants). This pioneering research had an animal behavior approach. During the 2000s, work on taxa-, clone- and kin-discrimination and recognition in protists produced genetic and molecular evidence that unicellular organisms (e.g. Saccharomyces, Dictyostelium, Polysphondylium, Tetrahymena, Entamoeba and Plasmodium) could distinguish between same (self or clone) and different (diverse clones), as well as among conspecifics of close or distant genetic relatedness. Here we discuss some of the research on the genetics of kin discrimination/recognition and highlight the scientific progress made by switching emphasis from investigating multicellular to unicellular systems (and backwards). We document how studies with protists are helping us to understand the microscopic, cellular origins and evolution of the mechanisms of kin discrimination/recognition and their significance for the advent of multicellularity. We emphasize that because protists are among the most ancient organisms on Earth, belong to multiple taxonomic groups and occupy all environments, they can be central to reexamining traditional hypotheses in the field of kin recognition, reformulating concepts, and generating new knowledge.

Discrimination Experiments in Entamoeba and Evidence from Other Protists Suggest Pathogenic Amebas Cooperate with Kin to Colonize Hosts and Deter Rivals

“…ability to discriminate/recognize taxa, clone, or kin, as observed in laboratory aggregation/segregation experiments (Espinosa and Paz‐y‐Miño‐C , ,b; Espinosa et al. ; Paz‐y‐Miño‐C and Espinosa , ), suggests that amebas use it during their life cycles to associate and cooperate preferentially with kin, and to deter genetically distant or unrelated rivals (i.e., potential cheaters). Because taxa, clone, and kin discrimination/recognition has been documented in a variety of unicellular eukaryotic lineages (Fig.…”

“…Although evidence of taxa and kin discrimination/recognition in invertebrates, vertebrates, and some plants has been gathered since the 1960s (references above), the advent of protists models into this field of research is new, early 2000s onwards (Espinosa and Paz‐y‐Miño‐C ; Paz‐y‐Miño‐C and Espinosa , ). Entamoeba species are among the least understood protists in terms of taxa, clone, and kin discrimination/recognition potential (Espinosa and Paz‐y‐Miño‐C , ,b).…”

“…have not been identified (we have searched for them in public databases: AmoebaDB, Entamoeba Welcome Sanger Institute, EnsemblProtists, NCBI, and UniProt; see links in references). To remain in intimate proximity, D. discoideum amebas rely on cell‐membrane adhesion proteins encoded by csA ; when wild‐type csA + cells are grown in mixed cultures with csA – knockouts, the amebas cluster preferentially with those equipped with fully functional adhesion polypeptides (Paz‐y‐Miño‐C and Espinosa , ; Queller et al. ).…”

“…SCIENTIFIC observations indicate that a large variety of unicellular eukaryotes (protists), members of major phylogenetic lineages, can tell apart same or self (clone/kin) from different or nonself (nonclone/nonkin). Indeed, protists have taxa, clone, and kin discrimination/recognition ability (Paz‐y‐Miño‐C and Espinosa , ). One of such protists is Entamoeba histolytica , an iconic Amoebozoa due to its relevance to human health (Fig.…”

“…). For comprehensive reviews of kin recognition in unicellular eukaryotes, as well as prokaryotes (bacteria and some archaea), see Espinosa and Paz‐y‐Miño‐C () and Paz‐y‐Miño‐C and Espinosa (, ).…”