David M. Rosenthal

Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers

Plant water-use efficiency (WUE) is expected to affect plant fitness and thus be under natural selection in arid habitats. Although many natural population studies have assessed plant WUE, only a few related WUE to fitness. The further determination of whether selection on WUE is direct or indirect through functionally related traits has yielded no consistent results. For natural populations of two desert annual sunflowers, Helianthus anomalus and H. deserticola, we used phenotypic selection analysis with vegetative biomass as the proxy for fitness to test (1) whether there was direct and indirect selection on WUE (carbon isotope ratio) and related traits (leaf N, area, succulence) and (2) whether direct selection was consistent with hypothesized drought/dehydration escape and avoidance strategies. There was direct selection for lower WUE in mesic and dry H. anomalus populations, consistent with dehydration escape, even though it is the longer lived of the two species. For mesic H. anomalus, direct selection favored lower WUE and higher N, suggesting that plants may be “wasting water” to increase N delivery via the transpiration stream. For the shorter lived H. deserticola in the direr habitat, there was indirect selection for lower WUE, inconsistent with drought escape. There was also direct selection for higher leaf N, succulence and leaf size. There was no direct selection for higher WUE consistent with dehydration avoidance in either species. Thus, in these natural populations of two desert dune species higher fitness was associated with some combination direct and indirect selection for lower WUE, higher leaf N and larger leaf size. Our understanding of the adaptive value of plant ecophysiological traits will benefit from further consideration of related traits such as leaf nitrogen and more tests in natural populations.

Phenotypic Differentiation between Three Ancient Hybrid Taxa and Their Parental Species

The primary requirement for a new diploid species to arise via hybridization is ecological divergence from its parental species. Ecological divergence protects the nascent hybrid species from competition with its progenitor species and may contribute to reproductive isolation. However, the means by which hybridization might facilitate the necessary adaptive transitions are poorly understood. Here, we report the results of a glasshouse experiment in which 42 morphological and ecophysiological traits were measured in three hybrid sunflower species (Helianthus anomalus, Helianthus deserticola, and Helianthus paradoxus) and their parental species (Helianthus annuus and Helianthus petiolaris). A surprisingly high proportion of traits were extreme relative to the parental species (24%, 20%, and 39% of traits in H. anomalus, H. deserticola, and H. paradoxus, respectively). Most of the extreme traits have previously been reported in the literature as adaptations to dune (H. anomalus), high‐desert (H. deserticola), or high‐salt (H. paradoxus) habitats. We propose that hybridization has contributed to ecological divergence largely via the generation of extreme traits in segregating hybrids, a commonly observed phenomenon called “transgressive segregation.”

SELECTION ON LEAF ECOPHYSIOLOGICAL TRAITS IN A DESERT HYBRID HELIANTHUS SPECIES AND EARLY-GENERATION HYBRIDS

Abstract Leaf ecophysiological traits related to carbon gain and resource use are expected to be under strong selection in desert annuals. We used comparative and phenotypic selection approaches to investigate the importance of leaf ecophysiological traits for Helianthus anomalus, a diploid annual sunflower species of hybrid origin that is endemic to active desert dunes. Comparisons were made within and among five genotypic classes: H. anomalus, its ancestral parent species (H. annuus and H. petiolaris), and two backcrossed populations of the parental species (designated BC2ann and BC2pet) representing putative ancestors of H. anomalus. Seedlings were transplanted into H. anomalus habitat at Little Sahara Dunes, Utah, and followed through a summer growing season for leaf ecophysiological traits, phenology, and fitness estimated as vegetative biomass. Helianthus anomalus had a unique combination of traits when compared to its ancestral parent species, suggesting that lower leaf nitrogen and greater leaf succulence might be adaptive. However, selection on leaf traits in H. anomalus favored larger leaf area and greater nitrogen, which was not consistent with the extreme traits of H. anomalus relative to its ancestral parents. Also contrary to expectation, current selection on the leaf traits in the backcross populations was not consistently similar to, or resulting in evolution toward, the current H. anomalus phenotype. Only the selection for greater leaf succulence in BC2ann and greater water‐use efficiency in BC2pet would result in evolution toward the current H. anomalus phenotype. It was surprising that the action of phenotypic selection depended greatly on the genotypic class for these closely related sunflower hybrids grown in a common environment. We speculate that this may be due to either phenotypic correlations between measured and unmeasured but functionally related traits or due to the three genotypic classes experiencing the environment differently as a result of their differing morphology.

Reconstructing the Origin of Helianthus deserticola: Survival and Selection on the Desert Floor

The diploid hybrid species Helianthus deserticola inhabits the desert floor, an extreme environment relative to its parental species Helianthus annuus and Helianthus petiolaris. Adaptation to the desert floor may have occurred via selection acting on transgressive, or extreme, traits in early hybrids between the parental species. We explored this possibility through a field experiment in the hybrid species’ native habitat using H. deserticola, H. annuus, H. petiolaris, and two populations of early‐generation (BC2) hybrids between the parental species, which served as proxies for the ancestral genotype of the ancient hybrid species. Character expression was evaluated for each genotypic class. Helianthus deserticola was negatively transgressive for stem diameter, leaf area, and flowering date, and the latter two traits are likely to be advantageous in a desert environment. The BC2 hybrids contained a range of variation that overlapped these transgressive trait means, and an analysis of phenotypic selection revealed that some of the selective pressures on leaf size and flowering date, but not stem diameter, would move the BC2 population toward the H. deserticola phenotype. Thus, H. deserticola may have originated from habitat‐mediated directional selection acting on hybrids between H. annuus and H. petiolaris in a desert environment.

Contrasting drought tolerance strategies in two desert annuals of hybrid origin

Woody plants native to mesic habitats tend to be more vulnerable to drought-induced cavitation than those in xeric habitats. Cavitation resistance in herbaceous plants, however, is rarely studied and whether or not annual plants in arid habitats conform to the trends observed in woody plants is unknown. This question is addressed by comparing the hydraulic properties of annual plants endemic to relatively mesic and seasonally xeric habitats in the Great Basin Desert, in both native and experimental settings. Vulnerability to cavitation between species differed as predicted when vulnerability curves of similar-sized native individuals were compared. Contrary to expectations, Helianthus anomalus from the relatively mesic dune sites, on average, exhibited higher native embolism, lower soil-to-leaf hydraulic conductance (kL) and lower transpiration rates, than its xeric analogue, H. deserticola. In transplant gardens, H. anomalus’ vulnerability to cavitation was unaffected by transplant location or watering treatment. In H. deserticola, however, vulnerability to cavitation varied significantly in response to watering in transplant gardens and varied as a function of stem water potential (Ψstem). H. deserticola largely avoided cavitation through its higher water status and generally more resistant xylem, traits consistent with a short life cycle and typical drought-escape strategy. By contrast, H. anomalus’ higher native embolism is likely to be adaptive by lowering plant conductance and transpiration rate, thus preventing the loss of root-to-soil hydraulic contact in the coarse sand dune soils. For H. anomalus this dehydration avoidance strategy is consistent with its relatively long 3–4 month life cycle and low-competition habitat. We conclude that variance of hydraulic parameters in herbaceous plants is a function of soil moisture heterogeneity and is consistent with the notion that trait plasticity to fine-grained environmental variation can be adaptive.