Evolution of Fitness Trade-Offs in Locally Adapted Populations of Pseudomonas fluorescens

Abstract

Local adaptation seems to be common in natural systems, but the genetic causes of its evolution remain poorly understood. Here we characterize the genetic causes of trade-offs generating local adaptation in populations of Pseudomonas fluorescens that had previously been evolved for specialization on three different carbon resources. We measured the fitness effects of mutations that arose during selection in that environment and in alternative environments to quantify the degree of specialization. We find that all mutations are beneficial in the environment of selection and that those arising later during adaptation are associated with increasingly antagonistic effects in alternative environments compared with those arising earlier, consistent with a multioptima version of Fisher's geometric model of adaptation. We also find that fitness of pairs of beneficial mutations are consistently less than additive in selection environments, producing a pattern of diminishing returns, but are more variable in alternative environments, being either positive or negative. Finally, we find that mutations in genes associated with loss of motility are beneficial across all environments, whereas mutations involving other functions, such as gene regulation, had more variable effects, being more environment specific. Taken together, these results provide a detailed account of the genetics of specialization and suggest that the evolution of trade-offs associated with local adaptation may often result from the antagonistic effects of beneficial mutations substituted later in adaptation.

Experimental evolution of the grain of metabolic specialization in yeast

“…This trend is consistent with a Fisher's geometric model of adaptation in a multipeaked landscape (Martin and Lenormand ; Schick et al. ).…”

“…It is worth mentioning that the negative response to on-pathway substrates displayed a tendency to become more negative through time (Table 1). This trend is consistent with a Fisher's geometric model of adaptation in a multipeaked landscape (Martin and Lenormand 2015;Schick et al 2015). This conclusion that specialization evolves among metabolic pathways is consistent with well-established trade-offs between major metabolic systems such as autotrophy versus heterotrophy (Reboud and Bell 1997) or fermentation versus respiration (Novak et al 2006;Frank 2010).…”

Fitness costs restrict niche expansion by generalist niche-constructing pathogens

“…All models that explore the conditions for the evolution and coexistence of specialists and generalists (for example, Wilson and Yoshimura, 1994;Egas et al, 2004;Abrams, 2006Abrams, , 2012Nurmi and Parvinen, 2008) assume that generalists trade off their ability to exploit multiple niches for their efficiency in any one. Indeed, were there no cost to being a generalist, generalists would always replace specialists, so the coexistence of these two strategies requires the existence of such costs, which are, however, seldom evaluated (Kassen, 2002;Palaima, 2007;Satterwhite and Cooper, 2015;Schick et al, 2015). Here, work with the plant pathogen Agrobacterium tumefaciens permits us to contribute new observations that help elucidate these questions of the evolution of generalist versus specialist strategies and competition and coexistence of the two types of strategies within their constructed niches.…”

Genomic evidence that resource-based trade-offs limit host-range expansion in a seed beetle

“…In other words, alleles that increase fitness in one environment are necessarily suboptimal in others (thus, trade-offs could contribute to the maintenance of variation within populations; Levene 1953;Huang et al 2014). Despite widespread evidence of local adaptation among populations (Leimu and Fischer 2008;Hereford 2009;Sanford and Kelly 2011), evidence for genetic trade-offs within populations has been more elusive, and most examples come from experimental evolution in microbial systems (e.g., Rodríguez-Verdugo et al 2014;Schick et al 2015). Without evidence for within-population fitness trade-offs, it is not possible to distinguish whether trade-offs are a cause or consequence of ecological specialization (Futuyma and Moreno 1988).…”