Christina M. Caruso

The evolution of the worldwide leaf economics spectrum

The worldwide leaf economic spectrum (WLES) is a strikingly consistent pattern of correlations among leaf traits. Although the WLES effectively summarizes variation in plant ecological strategies, little is known about its evolution. We reviewed estimates of natural selection and genetic variation for leaf traits to test whether the evolution of the WLES was limited by selection against unfit trait combinations or by genetic constraints. There was significant selection for leaf traits on both ends of the WLES spectrum, as well as significant genetic variation for these traits. In addition, genetic correlations between WLES traits were variable in strength and direction. These data suggest that genetic constraints have had a smaller role than selection in the evolution of the WLES.

Natural selection on floral traits of Lobelia (Lobeliaceae): spatial and temporal variation.

The strength and direction of natural selection on floral traits can vary spatially and temporally because of variation in the biotic and abiotic environment. High spatial variation in selection should lead to differentiation of floral traits among populations. In contrast, high temporal variation in selection should retard the evolution of population-specific floral phenotypes. To determine the relative importance of spatial vs. temporal variation in natural selection, we measured phenotypic selection on seven floral traits of the wildflowers Lobelia cardinalis and L. siphilitica in 1999 and 2000. Lobelia cardinalis experienced significant temporal variation in selection, whereas L. siphilitica experienced spatial variation in selection on the same traits. This variation in selection on floral traits was associated with spatial and temporal differences in the soil microenvironment. Although few studies of natural selection include spatial or temporal replicates, our results suggest that such replication is critical for understanding the distribution of phenotypes in nature.

PREDISPERSAL SEED HERBIVORES, NOT POLLINATORS, EXERT SELECTION ON FLORAL TRAITS VIA FEMALE FITNESS

Herbivores that oviposit in flowers of animal-pollinated plants depend on pollinators for seed production and are therefore expected to choose flowers that attract pollinators. This provides a mechanism by which seed herbivores and pollinators could impose conflicting selection on floral traits. We measured phenotypic selection on floral traits of Lobelia siphilitica (Lobeliaceae) via female fitness to determine the relative strength of selection by pollinators and a specialist predispersal seed herbivore. We were able to attribute selection on flowering phenology to the herbivores. However, no selection could be attributed to pollinators, resulting in no conflicting selection on floral traits. Unlike pollinators, whose preference for certain floral traits does not always translate into higher fitness, any discrimination by seed herbivores is likely to decrease fitness of the preferred floral phenotype. Thus predispersal seed herbivores may be a significant agent of selection on floral traits.

Plasticity of physiology in Lobelia: testing for adaptation and constraint.

Abstract Phenotypic plasticity is thought to be a major mechanism allowing sessile organisms such as plants to adapt to environmental heterogeneity. However, the adaptive value of many common plastic responses has not been tested by linking these responses to fitness. Even when plasticity is adaptive, costs of plasticity, such as the energy necessary to maintain regulatory pathways for plastic responses, may constrain its evolution. We used a greenhouse experiment to test whether plastic physiological responses to soil water availability (wet vs. dry conditions) were adaptive and/or costly in the congeneric wildflowers Lobelia cardinalis and L. siphilitica. Eight physiological traits related to carbon and water uptake were measured. Specific leaf area (SLA), photosynthetic rate (A), stomatal conductance (gs), and photosynthetic capacity (Amax) responded plastically to soil water availability in L. cardinalis. Plasticity in Amax was maladaptive, plasticity in A and gs was adaptive, and plasticity in SLA was adaptively neutral. The nature of adaptive plasticity in L. cardinalis, however, differed from previous studies. Lobelia cardinalis plants with more conservative water use, characterized by lower gs, did not have higher fitness under drought conditions. Instead, well‐watered L. cardinalis that had higher gs had higher fitness. Only Amax responded plastically to drought in L. siphilitica, and this response was adaptively neutral. We detected no costs of plasticity for any physiological trait in either L. cardinalis or L. siphilitica, suggesting that the evolution of plasticity in these traits would not be constrained by costs. Physiological responses to drought in plants are presumed to be adaptive, but our data suggest that much of this plasticity can be adaptively neutral or maladaptive.

Precipitation drives global variation in natural selection

Climate-driven selection Climate change will fundamentally alter many aspects of the natural world. To understand how species may adapt to this change, we must understand which aspects of the changing climate exert the most powerful selective forces. Siepielski et al. looked at studies of selection across species and regions and found that, across biomes, the strongest sources of selection were precipitation and transpiration changes. Importantly, local and regional climate change explained patterns of selection much more than did global change. Science, this issue p. 959 Local and regional climate changes in rainfall explain patterns of species selection across biomes more than global change. Climate change has the potential to affect the ecology and evolution of every species on Earth. Although the ecological consequences of climate change are increasingly well documented, the effects of climate on the key evolutionary process driving adaptation—natural selection—are largely unknown. We report that aspects of precipitation and potential evapotranspiration, along with the North Atlantic Oscillation, predicted variation in selection across plant and animal populations throughout many terrestrial biomes, whereas temperature explained little variation. By showing that selection was influenced by climate variation, our results indicate that climate change may cause widespread alterations in selection regimes, potentially shifting evolutionary trajectories at a global scale.

Sex ratio variation in gynodioecious Lobelia siphilitica: effects of population size and geographic location.

Variation in population sex ratio can be influenced by natural selection on alternate sex phenotypes as well as nonselective mechanisms, such as genetic drift and founder effects. If natural selection contributes to variation in population sex ratio, then sex ratio should covary with resource availability or herbivory. With nonselective mechanisms, sex ratio should covary with population size. We estimated sex ratio, resource availability, herbivory and size of 53 populations of gynodioecious Lobelia siphilitica. Females were more common in populations with higher annual temperatures, lower soil moisture and lower predation on female fruits, consistent with sex‐specific selection. Females were also more common in small populations, consistent with drift, inbreeding or founder effects. However, small populations occurred in areas with higher temperatures than large populations, suggesting that female frequencies in small populations could be caused by sex‐specific selection. Both selective and nonselective mechanisms likely affect sex ratio variation in this gynodioecious species.

Gender-specific floral and physiological traits: implications for the maintenance of females in gynodioecious Lobelia siphilitica.

A common gender dimorphism in angiosperms is gynodioecy, in which hermaphrodites and females co-occur. Females are at an inherent disadvantage because they can transmit their genes only through ovule production. One mechanism by which females can compensate for the loss of male function is by producing more seeds than hermaphrodites. As such, females should: (1) increase resource uptake to support higher seed production; and (2) allocate resources saved by the loss of male function to seed production. To test this hypothesis, we measured physiological and floral traits of gynodioecious Lobelia siphilitica, controlling for both environmental and genetic variation through a comparison of greenhouse-grown siblings. Pre-reproductive females had 14% higher area-based (Z=2.14; P=0.04) and 32% higher mass-based (Z=1.96; P=0.05) photosynthetic rate than hermaphrodites, suggesting that they have increased carbon acquisition by altering photosynthetic physiology. Female L. siphilitica produced flowers with 4–8% smaller corollas than hermaphrodites (all P<0.05), suggesting that females allocate resources away from floral structures used for pollinator attraction. The genetic correlation between genders for four floral and four physiological traits was significantly less than one but greater than zero, indicating that the evolution of gender dimorphism in response to sex-differential selection will be constrained. The allocation of resources saved by the loss of male function has been viewed as the most important mechanism allowing females of gynodioecious species to support higher seed production. Our data suggest that increased resource acquisition by females at pre-reproductive stages can also contribute to the maintenance of gender dimorphism in gynodioecious species.

POLLINATORS, HERBIVORES, AND THE MAINTENANCE OF FLOWER COLOR VARIATION: A CASE STUDY WITH LOBELIA SIPHILITICA

Conflicting selection by pollinators and herbivores is thought to be an important mechanism maintaining variation in flower color within plant populations. However, evidence for this mechanism is lacking because selection and the agents of selection on flower color have rarely been estimated. We estimated selection by pollinators and a predispersal seed predator on the three fundamental components of color (brightness, chroma, and hue) of Lobelia siphilitica flowers. We compared phenotypic selection on flowers of supplemental hand- versus open-pollinated plants to infer whether pollinators were an agent of selection on color. We compared attacked and unattacked plants to infer whether the seed predator was an agent of selection on color. Selection on brightness, but not chroma or hue, differed significantly between both pollination treatments and predation categories. Both pollinators and the seed predator exerted selection for less bright flowers, suggesting that they do not cause conflicting selection on flower color. However, we also detected phenotypic selection for brighter flowers that was not caused by pollinators or by the seed predator. Consequently, pollinators and herbivores are not sufficient to generate conflicting selection that could contribute to the maintenance of flower color variation in L. siphilitica.

Plasticity of inflorescence traits in Lobelia siphilitica (Lobeliaceae) in response to soil water availability

Many workers have demonstrated a genetic basis for variation in inflorescence traits, but this variation can also have an environmental component. Because flowering can incur significant water costs, I estimated plasticity of inflorescence traits of three populations of Lobelia siphilitica in response to drought. I manipulated soil water availability in the greenhouse and measured seven inflorescence traits. Under drought conditions, plants from one population flowered later and produced fewer flowers with shorter corollas and narrower landing pads. In contrast, the height of the flowering stalk decreased in response to drought in all three populations. Consequently, pollinator-mediated natural selection on these plastic traits may depend on soil water availability. Plastic responses differed between genotypes only for the height of the flowering stalk and the length of the corolla tube and only in one or two populations. This suggests that genotype × environment interactions would not limit the evolution of inflorescence traits in L. siphilitica. The strength and sign of phenotypic correlations among inflorescence traits did not respond plastically to drought, suggesting that indirect selection on inflorescence traits of L. siphilitica will not vary strongly with water availability. My results suggest that plasticity of inflorescence traits may influence their evolution, but the effects are population- and trait-specific.

Variation in resource limitation of plant reproduction influences natural selection on floral traits of Asclepias syriaca

The availability of both pollen and resources can influence natural selection on floral traits, but their relative importance in shaping floral evolution is unclear. We experimentally manipulated pollinator and resource (fertilizer and water) availability in the perennial wildflower Asclepias syriaca L. Nine floral traits, one male fitness component (number of pollinia removed), and two female fitness components (number of pollinia inserted and number of fruits initiated) were measured for plants in each of three treatments (unmanipulated control, decreased pollinator access, and resource supplementation). Although decreasing pollinators’ access to flowers did result in fewer pollinia inserted and removed, fruit set and phenotypic selection on floral traits via female and male fitness did not differ from the control. In contrast, resource supplementation increased fruit set, and phenotypic selection on seven out of nine floral traits was stronger via female than male fitness, consistent with the prediction that selection via female fitness would be greater when reproduction was less resource-limited. Our results support the hypothesis that abiotic resource availability can influence floral evolution by altering gender-specific selection.