Rapid and widespread de novo evolution of kin discrimination

Abstract

Diverse forms of kin discrimination, broadly defined as alteration of social behavior as a function of genetic relatedness among interactants, are common among social organisms from microbes to humans. However, the evolutionary origins and causes of kindiscriminatory behavior remain largely obscure. One form of kin discrimination observed in microbes is the failure of genetically distinct colonies to merge freely upon encounter. Here, we first use natural isolates of the highly social bacterium Myxococcus xanthus to show that colony-merger incompatibilities can be strong barriers to social interaction, particularly by reducing chimerism in multicellular fruiting bodies that develop near colony-territory borders. We then use experimental laboratory populations to test hypotheses regarding the evolutionary origins of kin discrimination. We show that the generic process of adaptation, irrespective of selective environment, is sufficient to repeatedly generate kin-discriminatory behaviors between evolved populations and their common ancestor. Further, we find that kin discrimination pervasively evolves indirectly between allopatric replicate populations that adapt to the same ecological habitat and that this occurs generically in many distinct habitats. Patterns of interpopulation discrimination imply that kin discrimination phenotypes evolved via many diverse genetic mechanisms and mutation-accumulation patterns support this inference. Strong incompatibility phenotypes emerged abruptly in some populations but strengthened gradually in others. The indirect evolution of kin discrimination in an asexual microbe is analogous to the indirect evolution of reproductive incompatibility in sexual eukaryotes and linguistic incompatibility among human cultures, the commonality being indirect, noncoordinated divergence of complex systems evolving in isolation. social evolution | nonself recognition | kin recognition | cooperation | territoriality T he behavior of many vertebrates (1, 2), invertebrates (3, 4) and microbes (5-7), as well as some plants (8), is altered by social encounters with conspecifics in a relatedness-dependent manner. Such kin discrimination is commonly interpreted in the context of inclusive fitness theory to have resulted from positive selection for kin discrimination per se (7, 9-11) specifically because such discrimination promotes preferential cooperation among kin that share cooperation alleles (12-14). However, despite any theoretical plausibility of kin selectionist explanations, the actual evolutionary origins of kin discrimination in natural populations are often difficult to infer due to their temporal remove (11,15). Kin discrimination, broadly defined (SI Appendix, Methods), might also arise indirectly as a byproduct of alternative evolutionary forces (15)(16)(17)(18)(19)(20). Despite decades of rigorous empirical and theoretical investigation of kin discrimination and its causes, a biological system that allows both the documentation of kin discrimination origins and causally proximate analys...

Kin discrimination between sympatric Bacillus subtilis isolates

“…For example, strains PS-20 and PS-160 had 100% identical housekeeping genes but still belonged to different recognition groups (4,5). This suggests that at least some of the loci responsible for kin discrimination may be under different evolutionary pressure than the phylogenetic markers.…”

“…A high frequency of swarming incompatibilities within a sympatric population suggests that kin discrimination occurred early during their evolutionary trajectory. The phenotypic variability of the boundary lines formed between swarms may imply that multiple loci or alleles are involved in kin discrimination, which might have evolved indirectly as byproducts of selection for some other traits (4). Further studies into the mechanisms behind B. subtilis kin discrimination should shed more light on its evolutionary origins.…”

“…However, kin selection may not be the only mechanism driving evolution of kin discrimination. In fact, recent work indicates that bacterial kin discrimination can also evolve indirectly, possibly as a byproduct of other adaptations (4). The phenomenon of kin discrimination has been studied from many different angles and in different organisms including animals (5), plants (6), social insects (7), amoeba (8,9), and bacteria (10).…”

“…The ability to discriminate between self and nonself during swarming was also studied in Myxobacteria, where incompatibility was always observed between unrelated strains (10). Incompatibility was even detected among some strains with 100% multilocus sequence tag identity (10) and was recently shown to evolve through modifications in many independent genetic loci (4).…”

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

“…Kin selection theory has proven to be a successful framework for addressing this question, with the central prediction that cooperation is favored by sufficient benefits to, and positive assortment between, cooperators (4)(5)(6)(7)(8). For example, recent study in experimental bacterial populations has elucidated mechanisms such as assortment emerging from limited or budding dispersal (9,10) and kin discrimination (11,12) that are consistent with kin selection fostering cooperative behaviors (e.g., refs. 8 and 13).…”