Environmentally induced responses co-opted for reproductive altruism

Abstract

Reproductive altruism is an extreme form of altruism best typified by sterile castes in social insects and somatic cells in multicellular organisms. Although reproductive altruism is central to the evolution of multicellularity and eusociality, the mechanistic basis for the evolution of this behaviour is yet to be deciphered. Here, we report that the gene responsible for the permanent suppression of reproduction in the somatic cells of the multicellular green alga, Volvox carteri , evolved from a gene that in its unicellular relative, Chlamydomonas reinhardtii , is part of the general acclimation response to various environmental stress factors, which includes the temporary suppression of reproduction. Furthermore, we propose a model for the evolution of soma, in which by simulating the acclimation signal (i.e. a change in cellular redox status) in a developmental rather than environmental context, responses beneficial to a unicellular individual can be co-opted into an altruistic behaviour at the group level. The co-option of environmentally induced responses for reproductive altruism can contribute to the stability of this behaviour, as the loss of such responses would be costly for the individual. This hypothesis also predicts that temporally varying environments, which will select for more efficient acclimation responses, are likely to be more conducive to the evolution of reproductive altruism.

Phylogeny and Molecular Evolution of the Green Algae

“…Although C. reinhardtii lacks an exact regA ortholog, phylogenetic analysis of the VARL gene family suggests that this is due to gene loss in the C. reinhardtii lineage rather than a gene duplication in the V. carteri lineage (Duncan et al, 2007). The most closely related C. reinhardtii regA homolog is induced under nutrient and light-deprivation, leading to the suggestion that the somatic differentiation function of regA was co-opted from an environmental acclimation function in the unicellular ancestor of V. carteri (Nedelcu & Michod, 2006;Nedelcu, 2009). …”

Volvocine Algae: From Simple to Complex Multicellularity

“…In addition, the mechanistic basis for the evolution of somatic cell differentiation (at least in V. carteri) can also be traced back to the ability of single-celled volvocine ancestors to temporarily repress their reproduction to increase survival, as part of their general photo-acclimation response to limiting or stressful conditions Nedelcu 2009b). However, the very same factors that allowed some lineages in this group to achieve high levels of complexity may have affected how complex they could become.…”

“…21) and the green alga Volvox carteri (Nedelcu 2009b). Likewise, genes involved in moss development have been found in the closest unicellular relatives of land plants .…”

“…This scenario implies that the evolution of somatic cell differentiation and the increase in complexity observed in the lineage leading to V. carteri involved changes in the regulatory elements of regA (whether regA has a role in somatic cell differentiation in the other Volvox species is not yet known). Furthermore, regA appears to have evolved from a regA-like gene already present in the unicellular ancestor of volvocine algae; its co-option might have involved changing its expression pattern from a temporal context (in response to environment) into a spatial (developmental) context Nedelcu 2009b).…”

Volvox: A simple algal model for embryogenesis, morphogenesis and cellular differentiation

“…Sequencing of gonidial-specific genes showed that 15 of the 19 encoded proteins were predicted to be involved in photosynthesis-related functions, suggesting that photosynthetic activity may be suppressed in somatic cells (Meissner et al, 1999). This finding has led to the idea that suppression of photosynthesis may be the primary mechanism for inducing a senescent fate in somatic cells, such that somatic cells are unable to grow sufficiently large or rapidly enough to reproduce (Kirk, 2001; Meissner et al, 1999; Michod, 2007; Nedelcu and Michod, 2004; Nedelcu, 2009). It should be noted, however, that information about comparative rates and productivity of photosynthesis in somatic versus gonidial cells is lacking, and that somatic cells have been shown to actively fix CO 2 (Pommerville and Kochert, 1982) and must also consume energy to maintain basal metabolism, flagellar motility and biosynthesis and secretion of ECM.…”