Hidden paths to endless forms most wonderful: Parasite-blind diversification of host quality

Abstract

Evolutionary diversification can occur in allopatry or sympatry, can be unselected or driven by selection, and can be phenotypically manifested immediately or remain phenotypically latent until later manifestation in a newly encountered environment. Diversification of host-parasite interactions is frequently studied in the context of intrinsically selective coevolution, but the potential for host-parasite interaction phenotypes to diversify latently during parasite-blind evolution is rarely considered. Here we use a social bacterium experimentally adapted to several environments in the absence of phage to analyse allopatric diversification of latent host quality - the degree to which a host population supports a viral epidemic. Phage-blind evolution reduced host quality overall, with some bacteria becoming completely resistant to growth suppression by phage. Selective-environment differences generated only mild divergence in host-quality. However, selective environments nonetheless played a major role in shaping evolution by determining the degree of stochastic diversification among replicate populations within treatments. Ancestral motility genotype was also found to strongly shape patterns of latent hostquality evolution and diversification. These outcomes show that adaptive landscapes can differ in how they constrain stochastic diversification of a latent phenotype and that major effects of selection on biological diversification can be missed by focusing on trait means. Collectively, our findings suggest that latent-phenotype evolution (LPE) should inform host-parasite evolution theory and that diversification should be conceived broadly to include latent phenotypes.

Hidden paths to endless forms most wonderful: Ecology latently shapes evolution of multicellular development in predatory bacteria

“…o latent phenotype 29,30 -a phenotype that is potentiated by a genotype but remains unmanifested until the causal genotype is exposed to an inductive environment. See Freund et al 30 for elaboration on use of the term 'latent-phenotype evolution' (LPE).…”

“…Replicate experimental populations evolving under the same selective pressures often diversify stochastically 87,88 . However, the character of the selective environment can limit the degree of such stochastic diversification, whether for immediately manifested or latent phenotypes 9,29,30,89 . For example, we have recently shown that social selection acting during M. xanthus development can limit the degree of stochastic morphological diversification among evolving populations 9 .…”

“…The relative origins and long-term evolutionary integration of the genetic systems enabling the motility, predation, aggregative development and germination components of myxobacterial multicellular life cycles remain to be thoroughly characterized 91,92 . However, the pervasiveness of LPE emergent from MyxoEE evolution experiments 29,30,56,57,59,60,74,84,86,93 and of pleiotropy across M. xanthus behaviors from mutations engineered or induced in mechanistic molecular studies 58,94 together indicate that many loci contribute to more than one of these behaviors. Increasingly systematic and extensive investigations of pleiotropy across M. xanthus behaviors under standardized conditions will provide greater insight into the shared vs. modular components of the genetic systems underlying these behaviors and their evolution 55 .…”

“…The likely contributions of LPE to long-term evolutionary processes have been receiving increasing attention [29][30][31][32][33]36 . The outcomes of MyxoEE-3 reported here suggest that not only LPE per se, but the ecological context in which LPE originates, may often be important for the evolution of many developmental systems.…”

“…adaptation or genetic drift) while the actual phenotype is only first manifested, and thus revealed to potential selection, after later exposure to an inductive environment. Such evolution of initially latent phenotypes -latent-phenotype evolution (LPE 29,30 , see Semantics in Methods) -is common [29][30][31][32][33] contributes to evolutionary diversification 29,30 and can fuel some forms of exaptation 26,[34][35][36] .…”