Ecotypes and Pathogen Races: Local Adaptation, Common Gardens, and Environmentally Induced Heritable Change

In terms of genetic variation among populations within a species, ecotypes or races are local matches between organism and environment. Among macroorganisms, they were first described in plants and subsequently have been well documented (Bradshaw 1972). Among microorganisms, races of fungal plant pathogens virulent at the level of “gene-for-gene” for specificity to host cultivars were described in the classic research by Flor (1956) beginning in the 1930s (recall Sidebar in Chap. 3 and rusts in Chap. 6).

Pathogen races are discriminated on the basis of their ability to infect one or more host genetic lines or cultivars. In plants, the ecotype/race form of genetic variation has traditionally been separated from phenotypic plasticity by various approaches, principally by either interchanging representatives of local populations or transplanting them to a common environment (‘common garden’ experiments; Clausen et al. 1948; Bradshaw 1959; Holeski et al. 2009), or by various in situ manipulations (Turkington and Harper 1979a,b; Linhart and Grant 1996). If the major attributes of such transplants are maintained when they are grown in a new situation, then the evidence is for the genotypic component of variation. The most common observation is that phenotypic and genotypic variation, acting together, produces some intermediate result.

There is extensive evidence for localized, genetically determined variation in many traits, for example with respect to heavy metal tolerance noted above, as well as to natural soil mosaics (e.g., Baythavong 2011), flowering time, nutritional and physiological responses, parasite resistance, competitive ability, and growth form along altitudinal gradients (examples summarized in Begon et al. 1996, pp. 39-46; Linhart and Grant 1996). Selection can be strong for such local specialization at spatial scales down to a few cm, and hence margins of the populations can be sharply drawn even in cases of substantial gene flow across them (Becker et al. 2008). Temporal differentiation also occurs among hosts and pathogens, as in the oscillation of plant subpopulations carrying resistance genes against certain pathogen races and conversely, the local distribution and prevalence of races in the pathogen population able to overcome the resistance (e.g., Burdon 1987a,b; Tack et al. 2012), though the temporal component in general has not been studied as extensively as spatial variation.

Some important generalities emerge from multiple studies on such genetic differentiation in plants. The first is that it arises from biotic and abiotic environmental heterogeneity that generates selection pressures (Linhart and Grant 1996). These different environments also can cause barriers to gene flow. The combined effects of heterogeneity and restricted gene flow tend to accentuate differentiation, particularly among relatively isolated subpopulations (an example being where exposed sites at higher altitudes affect phenology).

Can the environment directly impose heritable genetic change on organisms? This idea sounds heretical and a throwback to Lamarckism and the Lysenko era, but there is strong evidence that indeed this can happen in some cases. A good example is flax, where exposure of certain varieties to suboptimal growth conditions within a generation can result in progeny with properties distinct from their parents (Durrant 1962; Cullis 1983, 2005). Notably, the phenomenon in certain flax varieties is stable across generations (transgenerational), unlike many well-known epigenetic changes in plants that are expressed only within an individual (intraorganismal; see later discussion of epigenetics and Whittle et al. 2009; Ceccarelli et al. 2011). The differences include height and biomass, total nuclear DNA, and the number of genes coding for various RNAs (Walbott and Cullis 1985). Frequently, seeds from such plants breed true, producing stable lines (termed genotrophs by Durant 1962), regardless of their growth regimen.

These transitions are associated with changes in DNA evidently resulting in part from activation of transposable elements and can result in copy number variations. How widespread the flax phenomenon is phylogenetically remains unclear, as are all the genes and possibly epigenome involved, the underlying mechanisms, and evolutionary implications. Plants do seem to be genetically much more plastic than animals (Walbot and Cullis 1983; Heslop-Harrison and Schwarzacher 2011) and could change potentially in response to environmental stimuli in ways that animals cannot.