Christopher P. Krieg

Ferns exhibit extraordinary ecological diversity, and their independent gametophyte and sporophyte stages make them distinct among other plant groups, yet the extent to which gametophyte and sporophyte ecology are coordinated is unknown. Here, we integrated spatial and climatic data to test the hypothesis that independent fern gametophytes occupy novel climatic niche space relative to their sporophytes. We also examined the physiological mechanisms in the gametophyte life stage that may underpin spatial patterns of fern ecology. We discovered that 57% of species examined have gametophytes that occupy novel climate niche space relative to their sporophytes and that this expansion occurs along specific axes of climate variation. We also discovered evidence of strong convergence in gametophyte ecophysiological function across broad environmental gradients. In particular, we found that gametophyte photosynthetic rate per mass was strongly linearly correlated to atmospheric water demand (e.g., potential evapotranspiration) and monotonically correlated to precipitation inputs. Taken together, these discoveries represent previously uncharacterized ecology and potential mechanisms that may drive spatial patterns of fern biodiversity.

Ferns exhibit extraordinary ecological diversity, and their independent gametophyte and sporophyte stages make them distinct among other plant groups, yet the extent to which gametophyte and sporophyte ecology are coordinated is unknown. Here, we integrated spatial and climatic data to test the hypothesis that independent fern gametophytes occupy novel climatic niche space relative to their sporophytes. We also examined the physiological mechanisms in the gametophyte life stage that may underpin spatial patterns of fern ecology. We discovered that 57% of species examined have gametophytes that occupy novel climate niche space relative to their sporophytes and that this expansion occurs along specific axes of climate variation. We also discovered evidence of strong convergence in gametophyte ecophysiological function across broad environmental gradients. In particular, we found that gametophyte photosynthetic rate per mass was strongly linearly correlated to atmospheric water demand (e.g., potential evapotranspiration) and monotonically correlated to precipitation inputs. Taken together, these discoveries represent previously uncharacterized patterns and potential mechanisms that may drive spatial patterns of fern biodiversity.

Premise: Hybridization and polyploidization are common in vascular plants and important drivers of biodiversity by facilitating speciation and ecological diversification. A primary limitation to making broad synthetic discoveries in hybrid and allopolyploid biodiversity research is the absence of a standardized framework to compare data across studies and biological scales.Methods: Here, I present a new quantitative framework to investigate and interpret patterns in hybrid and allopolyploid biology called the divergence index (DI). The DI framework produces standardized data that are comparable across studies and variables. To show how the DI framework can be used to synthesize data, I analyzed published biochemical, physiological, and ecological trait data of hybrids and allopolyploids. I also apply key ecological and evolutionary concepts in hybrid and polyploid biology to translate nominal outcomes, including transgression, intermediacy, expansion, and contraction, in continuous DI space.Results: Biochemical, physiological, ecological, and evolutionary data can all be analyzed, visualized, and interpreted in the DI framework. The DI framework is particularly suited to standardize and compare variables with very different scales. When using the DI framework to understand niche divergence, a metric of niche overlap can be used to complement insights to centroid and breadth changes.Discussion: The DI framework is an accessible framework for hybrid and allopolyploid biology and represents a flexible and intuitive tool that can be used to reconcile outstanding problems in plant biodiversity research.

Global climate change and land use change underlie a need to develop new crop breeding strategies, and crop wild relatives (CWR) have become an important potential source of new genetic material to improve breeding efforts. Many recent approaches assume adaptive trait variation increases towards the relative environmental extremes of a species range, potentially missing valuable trait variation in more moderate or typical climates. Here, we leveraged distinct genotypes of wild chickpea (Cicer reticulatum) that differ in their relative climates from moderate to more extreme and perform targeted assessments of drought and heat tolerance. We found significance variation in ecophysiological function and stress tolerance between genotypes but contrary to expectations and current paradigms, it was individuals from more moderate climates that exhibited greater capacity for stress tolerance than individuals from warmer and drier climates. These results indicate that wild germplasm collection efforts to identify adaptive variation should include the full range of environmental conditions and habitats instead of only environmental extremes, and that doing so may significantly enhance the success of breeding programs broadly.

Tradeoffs between the energetic benefits and costs of traits can shape species and trait distributions along environmental gradients. Here we test predictions based on such tradeoffs using survival, growth, and 50 photosynthetic, hydraulic, and allocational traits of tenEucalyptusspecies grown in four common gardens along an 8-fold gradient in precipitation/pan evaporation (P/E_p) in Victoria, Australia. Phylogenetically structured tests show that most trait-environment relationships accord qualitatively with theory. Most traits appear adaptive across species within gardens (indicating fixed genetic differences) and within species across gardens (indicating plasticity). However, species from moister climates have lower stomatal conductance than others grown under the same conditions. Responses in stomatal conductance and five related traits appear to reflect greater mesophyll photosynthetic sensitivity of mesic species to lower leaf water potential. Our data support adaptive cross-over, with realized height growth of most species exceeding that of others in climates they dominate. Our findings show that pervasive physiological, hydraulic, and allocational adaptations shape the distributions of dominantEucalyptusspecies along a subcontinental climatic moisture gradient, driven by rapid divergence in speciesP/E_pand associated adaptations.

Premise: Plant ecological strategies are often defined by the integration of underlying traits related to resource acquisition, allocation, and growth. Correlations between key traits across diverse plants suggest that variation in plant ecological strategies is largely driven by a fast–slow continuum of plant economics. However, trait correlations may not be constant through the life of a leaf, and it is still poorly understood how trait function varies over time in long‐lived leaves.Methods: Here, we compared trait correlations related to resource acquisition and allocation across three different mature frond age cohorts in a tropical fern species, Saccoloma inaequale.Results: Fronds exhibited high initial investments of nitrogen and carbon, but with declining return in photosynthetic capacity after the first year. In the youngest fronds, we found water‐use efficiency to be significantly lower than in the oldest mature fronds due to increased transpiration rates. Our data suggest that middle‐aged fronds are more efficient relative to younger, less water‐use efficient fronds and that older fronds exhibit greater nitrogen investments without higher photosynthetic return. In addition, several trait correlations expected under the leaf economics spectrum (LES) do not hold within this species, and some trait correlations only appear in fronds of a specific developmental age.Conclusions: These findings contextualize the relationship between traits and leaf developmental age with those predicted to underlie plant ecological strategy and the LES and are among the first pieces of evidence for when relative physiological trait efficiency is maximized in a tropical fern species.

Cycadales is highly endangered and one of the oldest dioecious gymnosperm lineages, making their reproductive biology highly relevant to conservation efforts and our understanding of the impact of dioecy, yet cycad reproductive ecophysiology is poorly understood. We examined how the costs associated with reproduction may impact basic physiological variation in cycad species. Specifically, we measured traits related to functional morphology and photosynthetic physiology in sterile and fertile staminate plants (‘males’) of Zamia portoricensis. Light response curves showed that sterile plants had greater light-use efficiency and maximum photosynthetic capacity per area compared with fertile plants. However, fertile and sterile plants exhibited similar respiration rates. We found significantly more nitrogen in leaves of fertile individuals, but similar nitrogen isotope composition and no differences in carbon content between sterile and fertile individuals. Despite having lower leaf-level photosynthetic rates, fertile plants had greater canopy-level photosynthesis than sterile plants, which was achieved by increasing leaf number and total leaf area. Our data suggest that sterile individuals may have greater light demands relative to fertile individuals, and fertile individuals may have greater nitrogen demands, which may be critical for successful reproductive events in staminate plants of the endangered cycad, Z. portoricensis.

Conifers inhabit some of the most challenging landscapes where multiple abiotic stressors (e.g., aridity, freezing temperatures) often co-occur. Physiological tolerance to multiple stressors (‘poly-tolerance’) is thought to be rare because exposure to one stress generally limits responses to another through functional trade-offs. However, the capacity to exhibit poly-tolerance may be greater when combined abiotic stressors have similar physiological impacts, such as the disruption of hydraulic function imposed by drought or freezing. Here, we reviewed empirical data in light of theoretical expectations for conifer adaptations to drought and freeze–thaw cycles with particular attention to hydraulic traits of the stem and leaf. Additionally, we examined the commonality and spatial distribution of poly-stress along indices of these combined stressors. We found that locations with the highest values of our poly-stress index (PSi) are characterized by moderate drought and moderate freeze–thaw, and most of the global conifer distribution occupies areas of moderate poly-stress. Among traits examined, we found diverse responses to the stressors. Turgor loss point did not correlate with freeze–thaw or drought stress individually, but did with the PSi, albeit inverse to what was hypothesized. Leaf mass per area was more strongly linked with drought stress than the poly-stress and not at all with freeze–thaw stress. In stems, the water potential causing 50% loss of hydraulic conductivity became more negative with increasing drought stress and poly-stress but did not correlate with freeze–thaw stress. For these traits, we identified a striking lack of coverage for substantial portions of species ranges, particularly at the upper boundaries of their respective PSis, demonstrating a critical gap in our understanding of trait prevalence and plasticity along these stress gradients. Future research should investigate traits that confer tolerance to both freeze–thaw and drought stress in a wide range of species across broad geographic scales.

All green plants alternate between the gametophyte and sporophyte life stages, but only seed‐free vascular plants (ferns and lycophytes) have independent, free‐living gametophytes. Fern and lycophyte gametophytes are significantly reduced in size and morphological complexity relative to their sporophytic counterparts and have often been overlooked in ecological and physiological studies. Understanding the ecological and physiological factors that directly impact this life stage is of critical importance because the ultimate existence of a sporophyte is dependent upon successful fertilization in the gametophyte generation. Furthermore, previous research has shown that the dual nature of the life cycle and the high dispersibility of spores can result in different geographic patterns between gametophytes and their respective sporophytes. This variation in distribution patterns likely exacerbates the separation of selective pressures acting on gametophyte and sporophyte generations, and can uniquely impact a species’ ecology and physiology. Here, we provide a review of historical and contemporary methodologies used to examine ecological and physiological aspects of fern gametophytes, as well as those that allow for comparisons between the two generations. We conclude by suggesting methodological approaches to answer currently outstanding questions. We hope that the information covered herein will serve as a guide to current researchers and stimulate future discoveries in fern gametophyte ecology and physiology.