An official website of the United States government
ABSTRACT Widely documented in animals, behavioural thermoregulation mitigates negative impacts of climate change. Plants experience especially strong thermal variability but evidence for plant behavioural thermoregulation is limited. Along a montane elevation gradient,Argentina anserinaflowers warm more in alpine populations than at lower elevation. We linked floral temperature with phenotypes to identify warming mechanisms and documented petal movement and pollinator visitation using time‐lapse cameras. High elevation flowers were more cupped, focused light deeper within flowers and were more responsive to air temperature than low; cupping when cold and flattening when warm. At high elevation, a 20° increase in petal angle resulted in a 0.46°C increase in warming. Warming increased pollinator visitation, especially under cooler high elevation temperatures. A plasticity study revealed constitutive elevational differences in petal cupping and stronger temperature‐induced floral plasticity in high elevation populations. Thus, plant populations have evolved different behavioural responses to temperature driving differences in thermoregulatory capacity.
more »
« less
Divergent gametic thermal performance and floral warming across an elevation gradient
Abstract Thermal environments vary widely across species ranges, establishing the potential for local adaptation of thermal performance optima and tolerance. In the absence of local adaptation, selection should favor mechanisms to meet thermal optima. Floral temperature is a major determinant of reproductive success in angiosperms, yet whether gametic thermal performance shows signatures of local adaptation across temperature gradients, and how variation in gametic thermal performance influences floral evolution, is unknown. We characterized flowering season temperatures for the forb, Argentina anserina, at extremes of a 1000 m elevation gradient and generated thermal performance curves for pollen and ovule performance in populations at each extreme. Thermal optima fell between mean and maximum intrafloral temperatures. However, cooler high-elevation populations had ~4 °C greater pollen thermal optima than warmer low-elevation populations, while tolerance breadths did not differ. We then tested whether plants at elevational extremes differentially warmed the floral microenvironment. High-elevation flowers warmed significantly more than low, bringing intrafloral temperatures nearer the pollen optima. A manipulative experiment demonstrated that stronger warming in high elevation was conferred by floral tissues. Elevational divergence in floral warming may be driven, in part, by selection on flowers to meet different thermal demands of the gametophytes.
more »
« less
- Award ID(s):
- 2015459
- PAR ID:
- 10489157
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution
- ISSN:
- 0014-3820
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract The floral microenvironment impacts gametophyte viability and plant–pollinator interactions. Plants employ mechanisms to modify floral temperature, including thermogenesis, absorption of solar radiation, and evaporative cooling. Whether floral thermoregulation impacts reproductive fitness, and how floral morphological variation mediates thermoregulatory capacity are poorly understood.We measured temperature of the floral microenvironment in the field and tested for thermogenesis in the lab in early spring floweringHexastylis arifolia(Aristolochiaceae). We evaluated whether thermoregulatory capacity was associated with floral morphological variation. Finally, we experimentally determined the thermal optimum and tolerance of pollen to assess whether thermoregulation may ameliorate thermal stress to pollen.Pollen germination was optimal near 21 °C, with a 50% tolerance breadth of ~18 °C. In laboratory conditions, flowers exhibited thermogenesis of 1.5–4.8 °C for short intervals within a conserved timeframe (08:00–09:00 h). In the field, temperature inside the floral tube often deviated from ambient – floral interiors were up to 4 °C above ambient when it was cold, but some fell nearly 10 °C below ambient during peak heat. Flowers with smaller openings were cooler and more thermally stable than those with larger openings during peak heat. Thermoregulation maintained a floral microenvironment within the thermal tolerance breadth of pollen.Results suggest thatH. arifoliaflowers have a stronger capacity to cool than to warm, and that narrower floral openings create a distinct floral microenvironment, enhancing floral cooling effects. While deviation of floral temperature from ambient conditions maintains a suitable environment for pollen and suggests an adaptive role of thermoregulation, we discuss adaptive and nonadaptive mechanisms underlying floral warming and cooling.more » « less
-
Abstract 1. Critical thermal limits represent an important component of an organism's capacity to cope with future temperature changes. Understanding the drivers of variation in these traits may uncover patterns in physiological vulnerability to climate change. Local temperature extremes have emerged as a major driver of thermal limits, although their effects can be mediated by the exploitation of fine‐scale spatial variation in temperature through behavioural thermoregulation. 2. Here, we investigated thermal limits along elevation gradients within and between two cold‐water frog species (Ascaphusspp.), one with a coastal distribution (A. truei) and the other with a continental range (A. montanus). We quantified thermal limits for over 700 tadpoles, representing multiple populations from each species. We combined local temporal and fine‐scale spatial temperature data to quantify local thermal landscapes (i.e., thermalscapes), including the opportunity for behavioural thermoregulation. 3. Lower thermal limits for either species could not be reached experimentally without the water freezing, suggesting that cold tolerance is <0.3°C. By contrast, upper thermal limits varied among populations, but this variation only reflected local temperature extremes inA. montanus, perhaps as a consequence of the greater variation in stream temperatures across its range. Lastly, we found minimal fine‐scale spatial variability in temperature, suggesting limited opportunity for behavioural thermoregulation and thus increased vulnerability to warming for all populations. 4. By quantifying local thermalscapes, we uncovered different trends in the relative vulnerability of populations across elevation for each species. InA. truei, physiological vulnerability decreased with elevation, whereas inA. montanus, all populations were equally physiologically vulnerable. These results highlight how similar environments can differentially shape physiological tolerance and patterns of vulnerability of species, and in turn impact their vulnerability to future warming.more » « less
-
Flowering plants do not occur alone and often grow in mixed-species communities where pollinator sharing is high and interactions via pollinators can occur at pre- and post-pollination stages. While the causes and consequences of pre-pollination interactions have been well studied little is known about post-pollination interactions via heterospecific pollen (HP) receipt, and even less about the evolutionary implications of these interactions. In particular, the degree to which plants can evolve tolerance mechanisms to the negative effects of HP receipt has received little attention. Here, we aim to fill this gap in our understanding of post-pollination interactions by experimentally testing whether two co-flowering Clarkia species can evolve HP tolerance, and whether tolerance to specific HP ‘genotypes’ (fine-scale local adaptation to HP) occurs. We find that Clarkia species vary in their tolerance to HP effects. Furthermore, conspecific pollen performance and the magnitude of HP effects were related to the recipient's history of exposure to HP in C. xantiana but not in C. speciosa. Specifically, better conspecific pollen performance and smaller HP effects were observed in populations of C. xantiana plants with previous exposure to HP compared to populations without such exposure. These results suggest that plants may have the potential to evolve tolerance mechanisms to HP effects but that these may occur not from the female (stigma, style) but from the male (pollen) perspective, a possibility that is often overlooked. We find no evidence for fine-scale local adaptation to HP receipt. Studies that evaluate the adaptive potential of plants to the negative effects of HP receipt are an important first step in understanding the evolutionary consequences of plant–plant post-pollination interactions. Such knowledge is in turn crucial for deciphering the role of plant–pollinator interactions in driving floral evolution and the composition of co-flowering communities.more » « less
-
Chapman, Mark (Ed.)Abstract Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them “taller” biogeographic barriers.more » « less
