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A central issue in ecology is to understand the mechanisms that underlie the distributions of species. Climate is known to be a critical factor controlling the broad-scale distribution of organisms (Hutchinson, 1918; MacArthur, 1972; Grace, 1987; Iverson & Prasad, 1998; Rehfeldt et al., 1999, 2006; Cavender-Bares, 2005; Chuine, 2010), but often the physiological basis for climatic niche constraints is unknown. Linking the physiological tolerances of species to their climatic distributions is important in predicting future distributions of species under changing climatic conditions (Morin et al., 2007b). In particular, the freezing tolerance of species often corresponds to the minimum temperatures in their climate of origin (Sakai & Weiser, 1973; Woodward, 1990; Aizen & Woodcock, 1996), and the ability of different species to avoid or tolerate freezing stress through various mechanisms goes a long way to explain the geographic distributions of species (Parker, 1963; George et al., 1974; Latham & Ricklefs, 1993). It has long been hypothesized that the distributions of species are limited by freezing tolerance in the north (in the Northern Hemisphere) and by competition in the south (MacArthur, 1972). A potential mechanism underlying this hypothesis is a trade-off between growth rate and freezing tolerance (Woodward, 1987; Schenk, 1996; Loehle, 1998; Aitken & Hannerz, 2001). In the north, the acquisition of traits for cold acclimation and freezing tolerance has been hypothesized to impose a cost in terms of resource allocation that results in lower growth rates (Levitt, 1980; Beck, 1988; Körner & Larcher, 1988; Woodward, 1990; Howe et al., 2003); a lack of freezing tolerance at the southern edge of the species distribution thus permits higher growth rates and increased competitive ability (Woodward & Pigott, 1975; Woodward, 1987). More generally, increased tolerance to abiotic stress is believed to trade off against growth and competitive abilities in plants (Tilman, 1988) as a result of resource limitations that drive the evolution of allocation strategies. In addition to growth rate, seed mass is considered to be a critical life history attribute associated with season length that may limit southern distributions (Morin & Chuine, 2006). Seed mass contributes directly to absolute growth rates (Cavender-Bares et al., 2004) and is linked to increased survival and competitive ability (Kitajima & Fenner, 2000; Fenner & Thompson, 2005; Turnbull et al., 2008). Towards the tropics, higher seed mass may be favored by a longer season length, which allows a longer time for carbon accumulation, and may provide a competitive advantage in highly diverse tropical communities in which competitive interactions may dominate assembly processes. By contrast, seed mass may be constrained directly by season length at northern latitudes (Moles & Westoby, 2003; Chuine, 2010), or may be limited by resource investment in freezing tolerance, and large seeds may be less advantageous at northern latitudes where freezing stress is a dominant filter in community assembly.
From a historical biogeographic perspective, if species evolve in tropical regions with no freezing tolerance and then expand into the temperate zone, freezing tolerance may be acquired simultaneously with the evolution of slower growth during unfavorable periods, as both are thought to be advantageous in seasonally cold climates (Larcher & Bauer, 1981; Körner & Larcher, 1988; Kozlowski & Pallardy, 1997). Therefore, a negative relationship between freezing tolerance and growth rate could arise as a result of differential allocation of limited resources or of correlated evolution during range expansion from the tropics to the temperate zone, or both. For similar reasons, a negative relationship between freezing tolerance and seed size may also be expected. Variation in freezing tolerance, as well as both growth rates and seed size, among species could contribute to an explanation of range limits.
Within species, evidence of a decline in growth rate at more northern latitudes and colder temperatures is consistent across studies both in situ (Roberds et al., 1990; Matyas & Yeatman, 1992; Rehfeldt et al., 1999, 2001) and in common gardens (Smithberg & Weiser, 1968; Li et al., 1998; Oleksyn et al., 1998). In addition, several studies have shown a similar relationship across species (Rehfeldt, 1997; Yamahira & Conover, 2002; Green, 2007; Savage, 2010). Across species, seed size in forest species has been shown to increase towards the tropics and decrease at high latitudes (Moles & Westoby, 2003; Morin & Chuine, 2006).
A still debated question is whether populations within species show conservatism in their climatic tolerances, a perspective used to defend climatic niche modeling approaches (Wiens & Graham, 2005; Pearman et al., 2008). For example, freezing tolerance may have evolved conservatively, such that all populations within a species (or lineage) have the same resistance to freezing. Under this view, broadly distributed species exposed to a range of temperatures may be adapted to tolerate a wide range of climatic conditions with little local adaptation (Larcher, 2005). Many tree species can survive much colder freezing temperatures than occur in their current range (Fuchigami et al., 1971; Sakai & Weiser, 1973; Aitken & Adams, 1996), suggesting that freezing tolerance may not be costly to maintain in species with broad distributions. Woody species are known to have broad ecological distributions in comparison with herbaceous species, which have more specialized niches (Ricklefs & Latham, 1992). If species have broad and conserved climatic tolerances, little variation in climatic tolerances would be expected among populations.
Within species ranges, however, there is evidence that the distributions of plant species consist of populations genetically suited to local climates (Morgenstern, 1996; Aitken & Hannerz, 2001; Rehfeldt et al., 2001; Larcher, 2005; Cavender-Bares, 2007), and often show clinal variation in the climatic tolerances of species as a result of adaptive differentiation (Endler, 1977; Davis & Shaw, 2001; Rehfeldt et al., 2001; Howe et al., 2003). Clinal variation in freezing tolerance has been demonstrated in several tree species, suggesting high levels of local adaptation (Rehfeldt et al., 2001; Li et al., 2002; Aranda et al., 2005; Morin et al., 2007a; Friedman et al., 2008).
In this study, we examine growth, cold acclimation and freezing tolerance within and between four species in the live oak group (Quercus section Virentes) –Q. virginiana, Q. oleoides, Q. fusiformis and Q. geminata– in a common garden experiment. The live oaks are a small monophyletic lineage containing species in the southern USA and Central America. They are a useful group in which to examine the mechanisms underlying geographic distributions, because they span the tropical–temperate divide, with several species covering large latitudinal gradients. Previous studies have established genetic and morphological differentiation between Q. geminata and Q. virginiana (Cavender-Bares & Pahlich, 2009) and Q. virginiana and Q. oleoides (Cavender-Bares, 2007; Cavender-Bares et al., 2011), and there is evidence that the group originated in the tropics of Central America and subsequently expanded into the temperate zone (Cavender-Bares et al., 2011).
Our goals were to establish the extent to which the distributions of live oak species ranges were associated with cold acclimation, freezing tolerance and growth, consistent with the hypothesis that they are limited at the northern range by minimum temperature and at the southern range by competitive ability (growth rate), and whether live oak populations fit a model of local adaptation with narrow climatic tolerances, or of broad climatic tolerances with little variation among populations. We specifically tested, first, whether there was population- and/or species-level variation in the ability to cold acclimate. If more northern populations and/or species increased their freezing tolerance significantly under temperate conditions, but more southern populations did not, this provides evidence for the evolution of cold hardening in response to cold temperature cues. Second, we tested whether there was a trade-off between freezing tolerance and growth rate (both absolute and relative growth rates). A negative relationship, such that maternal lines with slower growth rates exhibit greater freezing tolerance, would provide evidence for this trade-off. We also examined the relationship between freezing tolerance and seed mass, because seed mass can influence competitive ability and has been predicted to vary with climatic distribution (Morin & Chuine, 2006). We note that shade tolerance can drive competitive outcomes in late successional forests (Bazzaz, 1979; Grime, 1979), but we did not examine it here, because all of the live oaks can be characterized as mid-successional savannah species that regenerate under similar (moderately high) light regimes (Kurz & Godfrey, 1962; Spector & Putz, 2006; Klemens et al., 2010). Finally, we tested the extent to which minimum temperatures at the population source predicted freezing tolerance and growth rate. Clinal variation in cold acclimation, freezing tolerance and growth rates among populations within species would provide evidence for local adaptation. Alternatively, large differences in freezing tolerance, growth rates and/or acclimation potential between species, but limited variation among populations within broadly distributed species, would indicate that species have conserved climatic niches and broad climatic tolerances.
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Fig. S1 Predicted species range for four live oak species based on precipitation and temperature.
Fig. S2 Leaf decline in Fv/Fm after freezing (− 10°C) and stem freezing injury at five freezing temperatures for temperate and tropical growth treatment.
Fig. S3 Regressions for leaf and stem freezing tolerance and absolute growth rate (AGR) and relative growth rate (RGR) for both temperate and tropical treatments.
Fig. S4 Mean acorn mass for species and populations.
Table S1 Acorn collection site locations for all maternal families
Table S2 Restricted maximum likelihood (REML) variance component estimates for all response variables for the amount of variation explained by species and population for each growth temperature treatment
Methods S1 Leaf and stem freezing method details.
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