Sex or cannibalism: Polyphenism and kin recognition control social action strategies in nematodes

Abstract

Resource polyphenisms, where single genotypes produce alternative feeding strategies in response to changing environments, are thought to be facilitators of evolutionary novelty. However, understanding the interplay between environment, morphology, and behavior and its significance is complex. We explore a radiation of Pristionchus nematodes with discrete polyphenic mouth forms and associated microbivorous versus cannibalistic traits. Notably, comparing 29 Pristionchus species reveals that reproductive mode strongly correlates with mouth-form plasticity. Male-female species exhibit the microbivorous morph and avoid parent-offspring conflict as indicated by genetic hybrids. In contrast, hermaphroditic species display cannibalistic morphs encouraging competition. Testing predation between 36 co-occurring strains of the hermaphrodite P. pacificus showed that killing inversely correlates with genomic relatedness. These empirical data together with theory reveal that polyphenism (plasticity), kin recognition, and relatedness are three major factors that shape cannibalistic behaviors. Thus, developmental plasticity influences cooperative versus competitive social action strategies in diverse animals.

Experimental and theoretical support for costs of plasticity and phenotype in a nematode cannibalistic trait

“…First, we measured the cost of phenotype by studying whether the formation of the predatory mouth morph negatively affects fecundity. We took advantage of the extensive collection of P. pacificus natural isolates and selected seven strains with intermediate mouth-morph ratios from across the P. pacificus phylogeny (Fig.1b)[27,34]. The ratios of these strains were considered intermediate since they were neither predominantly expressing the predatory (Eu) nor predominantly expressing the non-predatory (St) morph on the standard laboratory food source E. coli (Fig.…”

“…To measure the cost of phenotype, we took advantage of the extensive collection of P. pacificus natural isolates and selected seven strains with intermediate mouth-morph ratios from across the P. pacificus phylogeny (Fig.1b) (Rödelsperger et al . 2017; Lightfoot et al . 2021).…”

“…Cannibalism provides trophic and survival advantages by either extending energy resources or eliminating competition [43,44]. Evidently, the predatory mouth form in P. pacificus has proven to boost survivorship under severe conditions [45], and reduce competition on the basis of genomic relatedness [34]. Nevertheless, various P. pacificus natural isolates are either predominantly non-predatory, i.e ., St-biased, or intermediate.…”

Linking Molecular Mechanisms and Evolutionary Consequences of Resource Polyphenism

“…Not only do individuals of a species’ predatory morph kill individuals of other species at higher rates than they kill their own species, but even individual isolates (genotypes) of the same species kill other isolates at higher rates than their own (Lightfoot et al, 2019 ). Kin discrimination in this system largely depends on the identity of a hypervariable small peptide that is expressed in the nematodes’ body-wall epidermis (Lightfoot et al, 2019 ) and, otherwise, on overall genetic relatedness (Lightfoot et al, 2021 ). Although the cilia of anterior sensilla are required for prey assessment and environmental sensing in P. pacificus , self-recognition does not seem to require fully functioning cilia (Moreno et al, 2019 ), so it is not yet known how the peptide signal and genetic identity of others is detected.…”

“…Each of these steps of polyphenic development has its own challenges and opportunities for studying the molecular, ecological, and evolutionary bases and consequences of RP. For example, proximal mechanisms of kin recognition, an important feature of RP, can help inform evolutionary questions like what drives differences in social interaction strategies and reproductive mode (Lightfoot et al, 2021; see section ''Identification and Evolution of Environmental Sensing Mechanisms''). Determining the architecture of a developmental switch mechanism will enable predictions regarding the evolutionary outcomes of the phenotypes it regulates (see section ''Evolution and Mechanisms of Developmental Switches'').…”