Phenotypic plasticity and genetic diversity elucidate rarity and vulnerability of an endangered riparian plant

Abstract

Environmental change, accelerated by anthropogenic activities, threatens many species and can be especially challenging for rare species given their potentially limited capacity for migration and adaptation relative to more common species. The ability to acclimate via phenotypic plasticity could provide an important path to species persistence in the face of such change. We investigated the responses of an endangered plant species endemic to a highly dynamic riparian habitat in southeastern Tennessee, USA, and its most widespread congener to environmental change to elucidate their current statuses and future vulnerability. Specifically, we compared the population-and species-level plasticity of rare Pityopsis ruthii and common P. graminifolia to contrasting light, temperature, and water conditions in a growth chamber experiment to evaluate their potential to acclimate to environmental change. Contrary to our expectations, P. ruthii had greater phenotypic plasticity than its common congener in response to both altered light and water availability. But this plasticity was not associated with increased fitness, suggesting that it was not adaptive. Concurrently, we genotyped these individuals at nine putatively neutral microsatellite loci to contrast genetic diversity across the range of each species. As expected, P. ruthii exhibited reduced genetic diversity relative to its more common congener. Overall, our findings accord with the narrow range and current habitat specificity of P. ruthii, especially its tolerance of highly variable water, and highlight its potential vulnerability to future environmental change.

Eco‐evolutionary causes and consequences of rarity in plants: a meta‐analysis

“…Plant species can differ extensively in their plastic responses to environmental change (Sultan, 2000; Nicotra & Davidson, 2010; Godoy et al ., 2012; Dangremond et al ., 2015), and widespread species could have relatively high plasticity owing to greater spatial variation across their ranges (Murray et al ., 2002). Few studies explicitly contrasted plasticity across rare and common congeners (Liao et al ., 2006; Lovell & McKay, 2015; Hirst et al ., 2017; Rutherford et al ., 2017; Boyd et al ., 2022), even though numerous studies exposed rare and common species to multiple environmental conditions. Additionally, the plasticity studies in our dataset mostly neglected to test whether plasticity confers a fitness advantage in rare or common species (but see Boyd et al ., 2022), which is critical because plasticity can be a passive or maladaptive stress response (Palacio‐López et al ., 2015; Hendry, 2016; Bonser, 2021).…”

“…Few studies explicitly contrasted plasticity across rare and common congeners (Liao et al ., 2006; Lovell & McKay, 2015; Hirst et al ., 2017; Rutherford et al ., 2017; Boyd et al ., 2022), even though numerous studies exposed rare and common species to multiple environmental conditions. Additionally, the plasticity studies in our dataset mostly neglected to test whether plasticity confers a fitness advantage in rare or common species (but see Boyd et al ., 2022), which is critical because plasticity can be a passive or maladaptive stress response (Palacio‐López et al ., 2015; Hendry, 2016; Bonser, 2021). Studies that compare plasticity in rare and common species and link plasticity to performance in the context of probable environmental change could test the hypothesis that geographically restricted species or habitat specialists could be limited in their ability to acclimate to a broader range of environmental conditions.…”

“…Some studies described species rarity across multiple dimensions. For example, Pityopsis ruthii was described as ‘endemic’ given its narrow geographic distribution and habitat specialization to exposed boulders along just two rivers in Tennessee (Boyd et al ., 2022); we categorized this species along both of these axes of rarity for our analyses. In cases in which multiple studies of a single rare species described rarity differently, we elected to use the most restrictive description.…”

“…Additionally, rare species could exhibit low phenotypic plasticity (Murray et al ., 2002), which could restrict range expansions across variable environments and acclimation in situ to global change (Nicotra et al ., 2010). However, the degree of adaptive plasticity expressed by a rare species will depend on the extent of spatial and temporal heterogeneity in conditions, and rare species from more variable habitats can exhibit greater plasticity than their common congeners (Boyd et al ., 2022). To date, few studies have examined plasticity in the context of rarity (Liao et al ., 2006; Lovell & McKay, 2015; Rutherford et al ., 2017).…”

Phenotypic plasticity and genetic diversity shed light on endemism of rare Boechera perstellata and its potential vulnerability to climate warming

“…We included population as a random effect in these models. A significant interaction indicated that B. perstellata and B. laevigata responded differently to a change in the environmental factor (i.e., that the two species exhibited differences in plasticity; see Boyd, Odell, et al, 2022). To account for the numerous traits analyzed to assess plasticity, we used corrected p‐ values to minimize the false discovery rate (FDR; Benjamini & Hochberg, 1995).…”