Desiccation tolerance evolved recurrently across diverse plant lineages to enable survival in water-limited conditions. Many resurrection plants are polyploid, and several groups have hypothesized that polyploidy contributed to the evolution of desiccation tolerance. However, due to the vast phylogenetic distance between resurrection plant lineages, the rarity of desiccation tolerance, and the prevalence of polyploidy in plants, this hypothesis has been difficult to test. Here, we surveyed natural variation in morphological, reproductive, and desiccation tolerance traits across several cytotypes of a single species to test for links between polyploidy and increased resilience. We sampled multiple natural populations of the resurrection grass Microchloa caffra across an environmental gradient ranging from mesic to xeric in South Africa. We describe two distinct ecotypes of M. caffra that occupy different extremes of the environmental gradient and exhibit consistent differences in ploidy, morphological, reproductive, and desiccation tolerance traits in both field and common growth conditions. Interestingly, plants with more polyploid genomes exhibited consistently higher recovery from desiccation, were less reproductive, and were larger than plants with smaller genomes and lower ploidy. These data indicate that selective pressures in increasingly xeric sites may play a role in maintaining and increasing desiccation tolerance and are mediated by changes in ploidy.
- Award ID(s):
- 1906094
- NSF-PAR ID:
- 10332279
- Date Published:
- Journal Name:
- Plants
- Volume:
- 11
- Issue:
- 10
- ISSN:
- 2223-7747
- Page Range / eLocation ID:
- 1332
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Despite theoretical advances, the ecological factors and functional traits that enable species varying in seed size and fecundity to coexist remain unclear. Given inherent fecundity advantages, why don't small‐seeded species dominate communities?
In perennial grasslands, we evaluated whether small‐seeded species are less tolerant of competition from the community dominant bunchgrass than large‐seeded species, but also less vulnerable to seed predation by mice. We also explored whether trade‐offs involving competitive tolerance include two other functional traits, height and leaf mass per area (LMA). We added seeds of 17 forb species to plots where bunchgrass competition and rodent seed predation were manipulated across sites varying in bunchgrass productivity and thus competitive intensity. Seeds were added at densities mimicking interspecific variation in fecundity among target species.
Standardizing for differences in fecundity (i.e. seed input, which enabled us to evaluate inherent interspecific differences in susceptibility to biotic interactions), bunchgrass competition more greatly reduced recruitment and establishment of small‐ versus large‐seeded species, whereas rodent seed predation more greatly reduced the recruitment of large‐ versus small‐seeded species. Plant height and LMA were unrelated to the competition effect size.
Small‐seeded species abundance decreased across sites increasing in bunchgrass productivity, whereas this was not the case for large‐seeded species. For adult plants but not seedlings, community‐weighted functional trait means (CWM) for seed size, height and LMA increased in plots with versus without bunchgrass competition and the CWM for seed size and height also increased at sites with greater bunchgrass productivity (for adults only). In contrast, rodent seed predation had no significant effects on CWM seed size.
At the end of the experiment, adult abundance positively correlated with plant fecundity in plots lacking bunchgrass, indicating the inherent advantages accrued to high fecundity small‐seeded species. However, with bunchgrass competition, abundances were equalized across species due to reduced competitive tolerance of high fecundity small‐seeded species.
Synthesis . Our results suggest that coexistence among subordinate forb species varying in seed size and fecundity is in‐part due to a trade‐off involving competitive tolerance and fecundity, mediated by seed size and associated functional traits. -
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Abstract Plasticity in plant traits, including secondary metabolites, is critical to plant survival and competitiveness under stressful conditions. The ability of a plant to respond effectively to combined stressors can be impacted by crosstalk in biochemical pathways, resource availability and evolutionary history, but such responses remain underexplored. In particular, we know little about intraspecific variation in response to combined stressors or whether such variation is associated with the stress history of a given population.
Here, we investigated the consequences of combined water and herbivory stress for plant traits, including relative growth rate, leaf morphology and various measures of phytochemistry, using a common garden of
Asclepias fascicularis milkweeds. To examine how plant trait means and plasticities depend on the history of environmental stress, seeds for the experiment were collected from across a gradient of aridity in the Great Basin, United States. We then conducted a factorial experiment crossing water limitation with herbivory.Plants responded to water limitation alone by increasing the evenness of UV‐absorbent secondary metabolites and to herbivory alone by increasing the richness of metabolites. However, plants that experienced combined water and herbivory stress exhibited similar phytochemical diversity to well‐watered control plants. This lack of plasticity in phytochemical diversity in plants experiencing combined stressors was associated with a reduction in relative growth rates.
Leaf chemistry means and plasticities exhibited clinal variation corresponding to seed source water deficits. The total concentration of UV‐absorbent metabolites decreased with increasing water availability among seed sources, driven by higher concentrations of flavonol glycosides, which are hypothesized to act as antioxidants, among plants from drier sites. Plants sourced from drier sites exhibited higher plasticity in flavonol glycoside concentrations in response to water limitation, which increased phytochemical evenness, but simultaneous herbivory dampened plant responses to water limitation irrespective of seed source.
Synthesis . These results suggest that climatic history can affect intraspecific phytochemical plasticity, which may confer tolerance to water limitation, but that co‐occurring herbivory disrupts such patterns. Global change is increasing the frequency and intensity of stress combinations, such that understanding intraspecific responses to combined stressors is critical for predicting the persistence of plant populations. -
Environmental clines in organismal defensive traits are usually attributed to stronger selection by enemies at lower latitudes or near the host’s range center. Nonetheless, little functional evidence has supported this hypothesis, especially for coevolving plants and herbivores. We quantified cardenolide toxins in seeds of 24 populations of common milkweed ( Asclepias syriaca ) across 13 degrees of latitude, revealing a pattern of increasing cardenolide concentrations toward the host's range center. The unusual nitrogen-containing cardenolide labriformin was an exception and peaked at higher latitudes. Milkweed seeds are eaten by specialist lygaeid bugs that are even more tolerant of cardenolides than the monarch butterfly, concentrating most cardenolides (but not labriformin) from seeds into their bodies. Accordingly, whether cardenolides defend seeds against these specialist bugs is unclear. We demonstrate that Oncopeltus fasciatus (Lygaeidae) metabolized two major compounds (glycosylated aspecioside and labriformin) into distinct products that were sequestered without impairing growth. We next tested several isolated cardenolides in vitro on the physiological target of cardenolides (Na + /K + -ATPase); there was little variation among compounds in inhibition of an unadapted Na + /K + -ATPase, but tremendous variation in impacts on that of monarchs and Oncopeltu s. Labriformin was the most inhibitive compound tested for both insects, but Oncopeltus had the greater advantage over monarchs in tolerating labriformin compared to other compounds. Three metabolized (and stored) cardenolides were less toxic than their parent compounds found in seeds. Our results suggest that a potent plant defense is evolving by natural selection along a geographical cline and targets specialist herbivores, but is met by insect tolerance, detoxification, and sequestration.more » « less
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Environmental clines in organismal defensive traits are usually attributed to stronger selection by enemies at lower latitudes or near the host’s range center. Nonetheless, little functional evidence has supported this hypothesis, especially for coevolving plants and herbivores. We quantified cardenolide toxins in seeds of 24 populations of common milkweed (Asclepias syriaca) across 13 degrees of latitude, revealing a pattern of increasing cardenolide concentrations toward the host's range center. The unusual nitrogen-containing cardenolide labriformin was an exception and peaked at higher latitudes. Milkweed seeds are eaten by specialist lygaeid bugs that are even more tolerant of cardenolides than the monarch butterfly, concentrating most cardenolides (but not labriformin) from seeds into their bodies. Accordingly, whether cardenolides defend seeds against these specialist bugs is unclear. We demonstrate that Oncopeltus fasciatus (Lygaeidae) metabolized two major compounds (glycosylated aspecioside and labriformin) into distinct products that were sequestered without impairing growth. We next tested several isolated cardenolides in vitro on the physiological target of cardenolides (Na+/K+-ATPase); there was little variation among compounds in inhibition of an unadapted Na+/K+-ATPase, but tremendous variation in impacts on that of monarchs and Oncopeltus. Labriformin was the most inhibitive compound tested for both insects, but Oncopeltus had the greater advantage over monarchs in tolerating labriformin compared to other compounds. Three metabolized (and stored) cardenolides were less toxic than their parent compounds found in seeds. Our results suggest that a potent plant defense is evolving by natural selection along a geographical cline and targets specialist herbivores, but is met by insect tolerance, detoxification, and sequestration.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/plants11101332
