Maria Clara Castellanos

Anther Evolution: Pollen Presentation Strategies When Pollinators Differ

Male‐male competition in plants is thought to exert selection on flower morphology and on the temporal presentation of pollen. Theory suggests that a plant’s pollen dosing strategy should evolve to match the abundance and pollen transfer efficiency of its pollinators. Simultaneous pollen presentation should be favored when pollinators are infrequent or efficient at delivering the pollen they remove, whereas gradual dosing should optimize delivery by frequent and wasteful pollinators. Among Penstemon and Keckiella species, anthers vary in ways that affect pollen release, and the morphology of dried anthers reliably indicates how they dispense pollen. In these genera, hummingbird pollination has evolved repeatedly from hymenopteran pollination. Pollen production does not change with evolutionary shifts between pollinators. We show that after we control for phylogeny, hymenopteran‐adapted species present their pollen more gradually than hummingbird‐adapted relatives. In a species pair that seemed to defy the pattern, the rhythm of anther maturation produced an equivalent dosing effect. These results accord with previous findings that hummingbirds can be more efficient than bees at delivering pollen.

Comparative floral and vegetative differentiation between two European Aquilegia taxa along a narrow contact zone

As a first step in determining the identity and relative importance of the evolutionary forces promoting the speciation process in two closely related European taxa of Aquilegia, we investigated the levels of morphological variation in floral and vegetative characters over the narrow region where their ranges enter into contact, and evaluate the relative importance of both types of traits in their differentiation. A total of 12 floral and ten vegetative characters were measured on 375 plants belonging to seven A. vulgaris populations and six A. pyrenaica subsp. cazorlensis populations located in southeastern Spain. Floral and vegetative morphological differentiation occur between taxa and among populations within taxa, but only vegetative characters (particularly plant height and leaf petiolule length) contribute significantly to the discrimination between taxa. Differentiation among populations within taxa is mostly explained by variation in floral traits. Consequently, morphological divergence between the two taxa cannot be interpreted as an extension of among-population differences occurring within taxa. Multivariate vegetative, but not floral, similarity between populations could be predicted from geographical distance. Moreover, the key role of certain vegetative traits in the differentiation of A. vulgaris and A. p. cazorlensis could possibly be attributable to the contrasting habitat requirements and stress tolerance strategies of the two taxa. These preliminary findings seem to disagree with the currently established view of the radiation process in the genus Aquilegia in North America, where the differentiation of floral traits seems to have played a more important role.

Genetic component of flammability variation in a Mediterranean shrub

Recurrent fires impose a strong selection pressure in many ecosystems worldwide. In such ecosystems, plant flammability is of paramount importance because it enhances population persistence, particularly in non‐resprouting species. Indeed, there is evidence of phenotypic divergence of flammability under different fire regimes. Our general hypothesis is that flammability‐enhancing traits are adaptive; here, we test whether they have a genetic component. To test this hypothesis, we used the postfire obligate seeder Ulex parviflorus from sites historically exposed to different fire recurrence. We associated molecular variation in potentially adaptive loci detected with a genomic scan (using AFLP markers) with individual phenotypic variability in flammability across fire regimes. We found that at least 42% of the phenotypic variation in flammability was explained by the genetic divergence in a subset of AFLP loci. In spite of generalized gene flow, the genetic variability was structured by differences in fire recurrence. Our results provide the first field evidence supporting that traits enhancing plant flammability have a genetic component and thus can be responding to natural selection driven by fire. These results highlight the importance of flammability as an adaptive trait in fire‐prone ecosystems.

Intra-population comparison of vegetative and floral trait heritabilities estimated from molecular markers in wild Aquilegia populations.

Measuring heritable genetic variation is important for understanding patterns of trait evolution in wild populations, and yet studies of quantitative genetic parameters estimated directly in the field are limited by logistic constraints, such as the difficulties of inferring relatedness among individuals in the wild. Marker‐based approaches have received attention because they can potentially be applied directly to wild populations. For long‐lived, self‐compatible plant species where pedigrees are inadequate, the regression‐based method proposed by Ritland has the appeal of estimating heritabilities from marker‐based estimates of relatedness. The method has been difficult to implement in some plant populations, however, because it requires significant variance in relatedness across the population. Here, we show that the method can be readily applied to compare the ability of different traits to respond to selection, within populations. For several taxa of the perennial herb genus Aquilegia, we estimated heritabilities of floral and vegetative traits and, combined with estimates of natural selection, compared the ability to respond to selection of both types of traits under current conditions. The intra‐population comparisons showed that vegetative traits have a higher potential for evolution, because although they are as heritable as floral traits, selection on them is stronger. These patterns of potential evolution are consistent with macroevolutionary trends in the European lineage of the genus.

Meta-analysis of meta-analyses in plant evolutionary ecology

After two decades of meta-analyses on plant traits, we can now look for global emergent patterns in plant evolutionary ecology. Hundreds of meta-analyses have focused on the effects of specific selection pressures on plant fitness, and the buildup of such results allows us to ask general questions regarding selection pressures and plant responses, a major focus of evolutionary ecology. Plant traits are affected by both abiotic and biotic factors. For example, biotic pressures like herbivory may affect physiological (i.e. secondary defences) and reproductive (i.e. seed predation) traits. Similarly, abiotic pressures such as increased CO2 may affect both plant physiology and reproduction. We tested whether biotic or abiotic selective pressures are more important for plant traits, and if the strength of the response to those pressures depends on the plant trait studied by meta-analyzing published meta-analyses on plant responses. We classify meta-analyses according to the type of response variable studied (fitness and non-fitness traits) and the type of selective pressure examined (biotic or abiotic). Our database showed biases in the meta-analysis literature, for example that the majority of studies are focused on non-fitness traits, i.e. on traits that are not directly related to reproduction or survival, and furthermore, on non-fitness traits under abiotic selection pressures. The meta-meta-analysis showed that the strength of responses to selection depends on the nature of selection (stronger for biotic than for abiotic factors) but, unexpectedly, not on the type of trait under study as previously found. The stronger responses to biotic factors can be explained if biotic selection is more variable in space and time, driven by interactions with other organisms. The relative importance of biotic versus abiotic factors on plant traits has been little studied in the past, and would benefit from more studies and reviews that fill the under-represented combinations of selective pressures and plant traits (i.e. abiotic factors on fitness traits).

Meta-analysis of meta-analyses in plant evolutionary

After two decades of meta-analyses on plant traits, we can now look for global emergent patterns in plant evolutionary ecology. Hundreds of meta-analyses have focused on the effects of specific selection pressures on plant fitness, and the buildup of such results allows us to ask general questions regarding selection pressures and plant responses, a major focus of evolutionary ecology. Plant traits are affected by both abiotic and biotic factors. For example, biotic pressures like herbivory may affect physiological (i.e. secondary defences) and reproductive (i.e. seed predation) traits. Similarly, abiotic pressures such as increased CO2 may affect both plant physiology and reproduction. We tested whether biotic or abiotic selective pressures are more important for plant traits, and if the strength of the response to those pressures depends on the plant trait studied by meta-analyzing published meta-analyses on plant responses. We classify meta-analyses according to the type of response variable studied (fitness and non-fitness traits) and the type of selective pressure examined (biotic or abiotic). Our database showed biases in the meta-analysis literature, for example that the majority of studies are focused on non-fitness traits, i.e. on traits that are not directly related to reproduction or survival, and furthermore, on non-fitness traits under abiotic selection pressures. The meta-meta-analysis showed that the strength of responses to selection depends on the nature of selection (stronger for biotic than for abiotic factors) but, unexpectedly, not on the type of trait under study as previously found. The stronger responses to biotic factors can be explained if biotic selection is more variable in space and time, driven by interactions with other organisms. The relative importance of biotic versus abiotic factors on plant traits has been little studied in the past, and would benefit from more studies and reviews that fill the under-represented combinations of selective pressures and plant traits (i.e. abiotic factors on fitness traits).

Field heritability of a plant adaptation to fire in heterogeneous landscapes.

The strong association observed between fire regimes and variation in plant adaptations to fire suggests a rapid response to fire as an agent of selection. It also suggests that fire‐related traits are heritable, a precondition for evolutionary change. One example is serotiny, the accumulation of seeds in unopened fruits or cones until the next fire, an important strategy for plant population persistence in fire‐prone ecosystems. Here, we evaluate the potential of this trait to respond to natural selection in its natural setting. For this, we use a SNP marker approach to estimate genetic variance and heritability of serotiny directly in the field for two Mediterranean pine species. Study populations were large and heterogeneous in climatic conditions and fire regime. We first estimated the realized relatedness among trees from genotypes, and then partitioned the phenotypic variance in serotiny using Bayesian animal models that incorporated environmental predictors. As expected, field heritability was smaller (around 0.10 for both species) than previous estimates under common garden conditions (0.20). An estimate on a subset of stands with more homogeneous environmental conditions was not different from that in the complete set of stands, suggesting that our models correctly captured the environmental variation at the spatial scale of the study. Our results highlight the importance of measuring quantitative genetic parameters in natural populations, where environmental heterogeneity is a critical aspect. The heritability of serotiny, although not high, combined with high phenotypic variance within populations, confirms the potential of this fire‐related trait for evolutionary change in the wild.

Bee- to bird-pollination shifts in Penstemon: effects of floral-lip removal and corolla constriction on the preferences of free-foraging bumble bees

Plants might be under selection for both attracting efficient pollinators and deterring wasteful visitors. Particular floral traits can act as exploitation barriers by discouraging the unwelcome visitors. In the genus Penstemon, evolutionary shifts from insect pollination to more efficient hummingbird pollination have occurred repeatedly, resulting in the convergent evolution of floral traits commonly present in hummingbird-pollinated flowers. Two of these traits, a reduced or reflexed lower petal lip and a narrow corolla, were found in a previous flight-cage study to affect floral handling time by bumble bees, therefore potentially acting as “anti-bee” traits affecting preference. To test whether these traits do reduce bumble bee visitation in natural populations, we manipulated these two traits in flowers of bee-pollinated Penstemon strictus to resemble hummingbird-adapted close relatives and measured the preferences of free-foraging bees. Constricted corollas strongly deterred bee visitation in general, and particularly reduced visits by small bumble bees, resulting in immediate specialization to larger, longer-tongued bumble bees. Bees were also deterred—albeit less strongly—by lipless flowers. However, we found no evidence that lip removal and corolla constriction interact to further affect bee preference. We conclude that narrow corolla tubes and reduced lips in hummingbird-pollinated penstemons function as exploitation barriers that reduce bee access to nectaries or increase handling time.

Can facilitation influence the spatial genetics of the beneficiary plant population

1. Plant facilitation is a positive interaction where a nurse or nurse plant community alters the local conditions, improving the life-time fitness of other beneficiary plants. In stressful environments, a common consequence is the formation of discrete vegetation patches under nurse plants, surrounded by open space. The consequences of such spatial patterns have been studied mostly at the community level. 2. At the population level, facilitation causes a distribution of beneficiary individuals that could have intra-specific genetic consequences. The spatial patchiness and the increase in local aggregation can potentially affect the population fine-scale genetic structure. In addition, marked microenvironmental differences under nurses versus outside could lead to plastic phenotypic variation between facilitated and non-facilitated individuals, as for example reproductive asynchrony, potentially producing assortative mating. 3. This study tests the hypothesis that plant facilitation can have genetic consequences for the population of a beneficiary plant (Euphorbia nicaeensis) by affecting its spatial genetic structure and mating patterns between subpopulations of facilitated and non-facilitated individuals. 4. Facilitation in this system creates an aggregated distribution of beneficiary individuals compared to a minority of non-facilitated individuals that grow on the open ground. Facilitation also leads to slight phenological differences mediated by strong microenvironmental differences created by nurses compared to the open ground. Yet a molecular analysis showed that, although there is fine scale spatial genetic structure in this system, there is no evidence that it is caused by facilitation. Numerical simulations further showed that spatial genetic patterns in the population are little influenced by the phenological mismatch observed in the field. 5. Synthesis. Facilitation leads to the strong spatial aggregation of beneficiary plants and desynchronizes their flowering phenology, but the magnitude of these effects is not enough to have local genetic consequences in our study system. Facilitation seems thus to have a homogenizing role by allowing the persistence of a diverse gene pool in populations in harsh environments, rather than fomenting genetic differentiation. Further information on other systems where facilitation produces stronger spatial or phenological effects on facilitated plants is needed to fill the large knowledge gap we have on the genetic effects of facilitation.

Intra-population comparison of vegetative and floral trait

Measuring heritable genetic variation is important for understanding patterns of trait evolution in wild populations, and yet studies of quantitative genetic parameters estimated directly in the field are limited by logistic constraints, such as the difficulties of inferring relatedness among individuals in the wild. Marker‐based approaches have received attention because they can potentially be applied directly to wild populations. For long‐lived, self‐compatible plant species where pedigrees are inadequate, the regression‐based method proposed by Ritland has the appeal of estimating heritabilities from marker‐based estimates of relatedness. The method has been difficult to implement in some plant populations, however, because it requires significant variance in relatedness across the population. Here, we show that the method can be readily applied to compare the ability of different traits to respond to selection, within populations. For several taxa of the perennial herb genus Aquilegia, we estimated heritabilities of floral and vegetative traits and, combined with estimates of natural selection, compared the ability to respond to selection of both types of traits under current conditions. The intra‐population comparisons showed that vegetative traits have a higher potential for evolution, because although they are as heritable as floral traits, selection on them is stronger. These patterns of potential evolution are consistent with macroevolutionary trends in the European lineage of the genus.