The many examples of convergence and parallel evolution in similar environments are some of the most striking examples of evolution by natural selection, suggesting that species respond similarly to the same environmental selection pressures. The repeated evolution of succulence in plants from arid environments, for example, reflects the consequences of natural selection for water storage in arid environments (Beard, 1976; Ogburn & Edwards, 2010). Similarly, the repeated evolution of benthic and limnetic forms of fish (sticklebacks, lake whitefish, pumpkinseed, and bluegill sunfish) in post-glacial lakes is the result of character displacement in response to competition in the newly created lake habitats (reviewed by Schluter & McPhail, 1993).
We recognize less often that species may respond to the same selection pressure in different ways. For example, within Drosophila melanogaster, Cohan & Hoffmann (1986) found similar responses to selection for ethanol tolerance in replicate experimental populations, but the genetic underpinnings of the ethanol tolerance differed from one replicate to another. The fitness associated with different genotypes at the alcohol dehydrogenase locus depended on the pre-existing genetic background of the individuals. Similarly, Young et al. (2007) showed that shrews with similar diets have functionally similar, but morphologically divergent, jaw structures. Thus, different morphologies may also be the result of similar selection (Young et al., 2007). Even in cases where convergent evolution is well documented, the unique evolutionary history of individual lineages may play a role in how each lineage adapts to its environment. For example, in the radiation of Anolis lizards on Caribbean islands, crown giant anoles on the island of Puerto Rico tend to have narrower pectoral width, deeper heads and wider pelvic widths than crown giant anoles on other islands (Langerhans et al., 2006). There are even examples where apparently adaptive responses to the same environmental selection arise from trait responses in opposite directions. For example, Nakazato et al. (2008) found that in two species of Andean tomatoes, the between-population associations of plant height with elevation and of days to wilting with mean annual precipitation were similar between species. In contrast, the association of leaf area with elevation depended on the species examined. In Solanum pimpinellifolium, plants tended to have larger leaves in the higher-elevation population, and in Solanum lycopersicum var. cerasiforme, plants tended to have smaller leaves in the higher-elevation population. Differential responses to apparently similar selection pressures could reflect lineage-specific differences in genetic variances and covariances between traits (Arnold et al., 2008; Hanson & Houle, 2008), the vagaries of genetic drift and independent mutational histories (Travisano et al., 1995), or subtle differences in the environment that were not measured. Different adaptive responses, although affected by nonadaptive forces, are ultimately driven by natural selection to a landscape that has multiple optima.
Large-scale trait–environment associations are often attributed to the effects of natural selection. For example, plants from drier and more nutrient-poor areas tend to have thicker or denser leaves (Cunningham et al., 1999; Fonseca et al., 2000; Niinemets, 2001), plant height is correlated with precipitation (Moles et al., 2009), and rooting depth increases with increasing drought (Canadell et al., 1996) and rainfall seasonality (Schenk & Jackson, 2002). All of these associations have been interpreted as adaptive responses to the environment, and these large-scale patterns suggest that species respond predictably to variation along these environmental gradients. Similarly, trait–environment associations between populations within species are often interpreted as adaptations to the local environment (Endler, 1986), but the extent to which these large-scale patterns are reflected within species is less explored.
In this study, we investigated a small evolutionary radiation to determine whether trait variation among populations within species is associated with similar environmental gradients across species and whether this trait variation reflects large-scale trait–environment associations (Table 1). Specifically, we investigated trait–environment associations within the white proteas (Protea sect. Exsertae), a group of six closely related species endemic to the mountains of South Africa that diverged recently (0.34–1.2 Myr; Valente et al., 2010). While the species are almost completely allopatric, they have broad environmental tolerances (Latimer et al., 2009) and do not cleanly partition environmental space (Fig. 1; see also Latimer et al., 2006). In fact, as Latimer et al. (2009) showed, the differences between species in their mean environments are not enough to account for the almost complete allopatry in this group, suggesting that adaptive differences between populations – in addition to differences between species – may contribute significantly to the diversity of the group (Carlson et al., 2011).
|Expected Trait–environment correlation||Citation||Trait||Environment||Supported in our study?|
|Biomass decreases as elevation increases||Clausen et al., (1940)||Root mass, shoot mass, shoot height, leaves present||COLDPCA||+P. mundii, +P. punctata, + P. lacticolor, −P. aurea|
|Root/shoot ratio increases with decreased rainfall||Schenk & Jackson (2002)||Root mass/shoot mass||DRYPCA||+ P. mundii|
|Leaves become larger and wider with increased rainfall||Cunningham et al. (1999)||LWR||DRYPCA||+P. aurea and +P. mundii|
|Plant height increases with increased rainfall||Moles et al. (2009)||Shoot height||DRYPCA||No|
|Roots length increases with increased drought||Canadell et al. (1996)||Root length||DRYPCA||No|
|SLA increases with increased rainfall||Wright et al. (2004)||SLA||DRYPCA||No|
|Seeds are larger in lower-nutrient soils||Beadle (1966)||Seed mass||FERTPCA||No|
|Proteoid roots increase with decreased soil fertility||Lamont (1982)||Proteoid roots||FERTPCA||No|
|SLA decreases with decreased soil fertility||Cunningham et al. (1999)||SLA||FERTPCA||No|
|Root branching increases with more concentrated rainfall||Nicotra et al. (2002)||Root length/root mass||PPTCON||+ P. mundii,−P. aurea|
|Root depth increases with increasing rainfall seasonality||Schenk & Jackson (2002)||Root length||PPTCON||+P. subvestita|
Our previous work on the white proteas found that among-population differences in leaf traits are adaptively associated with climate, for example thick or dense leaves appear to be adaptations to a harsh climate (Carlson et al., 2011). These results are consistent with expectations from large-scale surveys of trait–environment correlations across all flowering plant species (Wright et al., 2004). Differences in traits associated with access to nutrients and water and differences in seed size are also likely important foci of adaptation in most plants, including the white proteas. The environments in which the white proteas grow vary widely in the timing and amount of rainfall (Schultze, 2007), in hydrological conditions and in soil nutrients (Specht & Moll, 1983; Witkowski & Mitchell, 1987). In proteas, long tap roots are needed to reach the water table (Richards et al., 1995; Watt & Evans, 1999), and access to nutrients is facilitated by the production of proteoid roots, specialized cluster roots on lateral roots. Proteoid roots are especially important for uptake of phosphorous (Lamont, 1982; Neumann & Martinoia, 2002), but they also enhance uptake of nitrogen and micronutrients (Jeschke & Pate, 1995). Similarly, large seeds have been found to be adaptive in low-nutrient conditions (due to better provisioning; Beadle, 1966), both within (Bonfil & Kafkafi, 2000; Vaughton & Ramsey, 2001) and across species (Milberg et al., 1998; Shane et al., 2008).
Here we use leaf, shoot and root traits measured in a common environment to answer the following questions: (i) Does evolutionary history, similar evolutionary responses to the environment or lineage-specific evolutionary responses to the environment play a larger role in the trait diversification of the white proteas? (ii) What traits are associated with lineage-specific evolutionary responses to the environment? (iii) Do the species-specific trait–environment associations reflect large-scale trait–environment correlations?