Benoit Pujol

The evolutionary ecology of clonally propagated domesticated plants.

While seed-propagated crops have contributed many evolutionary insights, evolutionary biologists have often neglected clonally propagated crops. We argue that widespread notions about their evolution under domestication are oversimplified, and that they offer rich material for evolutionary studies. The diversity of their wild ancestors, the diverse ecologies of the crop populations themselves, and the intricate mix of selection pressures, acting not only on the parts harvested but also on the parts used by humans to make clonal propagules, result in complex and diverse evolutionary trajectories under domestication. We examine why farmers propagate some plants clonally, and discuss the evolutionary dynamics of sexual reproduction in clonal crops. We explore how their mixed clonal/sexual reproductive systems function, based on the sole example studied in detail, cassava (Manihot esculenta). Biotechnology is now expanding the number of clonal crops, continuing the 10 000-yr-old trend to increase crop yields by propagating elite genotypes. In an era of rapid global change, it is more important than ever to understand how the adaptive potential of clonal crops can be maintained. A key component of strategies for preserving this adaptive potential is the maintenance of mixed clonal/sexual systems, which can be achieved by encouraging and valuing farmer knowledge about the sexual reproductive biology of their clonal crops.

Reduced inbreeding depression after species range expansion

Many species expanded their geographic ranges from core “refugium” populations when the global climate warmed after the Pleistocene. The bottlenecks that occur during such range expansions diminish genetic variation in marginal populations, rendering them less responsive to selection. Here, we show that range expansion also strongly depletes inbreeding depression. We compared inbreeding depression among 20 populations across the expanded range of a common European plant, and found that marginal populations had greatly reduced inbreeding depression. Similar patterns were also revealed by multilocus computer simulations. Low inbreeding depression is predicted to ease conditions for the evolution of self-fertilization, and selfing is known to be particularly frequent in marginal populations. Therefore, our findings expose a remarkable aspect of evolution at range margins, where a history of expansion can reverse the direction of selection on the mating system, providing a parsimonious explanation for the high incidence of selfing in marginal populations.

Germination Ecology of Cassava (Manihot Esculenta Crantz, Euphorbiaceae) in Traditional Agroecosystems: Seed and Seedling Biology of a Vegetatively Propagated Domesticated Plant1

Cassava is clonally propagated, but Amerindian farmers also use plants from volunteer seedlings to prepare stem cuttings. Although sexual reproduction plays a role in cassava’s evolution it is poorly studied. We examined one aspect of cassava reproductive ecology, seed dormancy and germination. Volunteer seedlings emerge from a soil bank of seeds produced during the previous cycle of cultivation that remain ungerminated through the fallow period, then germinate synchronously after vegetation is slashed and burned. Laboratory experiments showed that germination can be enhanced by mechanical scarification and also by dry heat treatment, suggesting that burning after field clearing could help break dormancy. Germination was also stimulated by high temperatures (35°C) that in nature indicate bare soils, and inhibited by temperatures (25°C) close to those in soil shaded by vegetation and by light. Seeds of both wild and domesticated cassava exhibit physiological dormancy, an adaptation for germination in periodically disturbed habitats. In addition to these preadaptations, preliminary results also suggest specific adaptations of domesticated cassava to the distinctive disturbance regimes of swidden agriculture.

GENDER VARIATION AND TRANSITIONS BETWEEN SEXUAL SYSTEMS IN MERCURIALIS ANNUA (EUPHORBIACEAE)

Evolutionary transitions between hermaphroditism and dioecy have occurred numerous times in the land plants. We briefly review the factors thought to be responsible for these transitions, and we provide a synthesis of what has been learned from recent studies of the annual herb Mercurialis annua, in which dioecy (males and females), monoecy (functional hermaphrodites), and androdioecy (males and hermaphrodites) occur in different parts of its geographic range. Previous research on M. annua has revealed the importance of genome duplication and hybridization in the origin of much of the observed variation. Here we show, however, that spatial transitions in the sexual system also occur within the same ploidy level. In particular, we present an analysis, using flow cytometry data, of ploidy variation across a previously unstudied transition between hermaphroditism and androdioecy, in which we find that the sexual‐system transition is uncoupled from the shift in ploidy levels. We review recent research that shows that such transitions between sexual systems in M. annua are consistent with differential selection at the regional level for reproductive assurance during colonization. We also present new experimental data that highlight both the importance of the resource status of plants and that of their local mating context in regulating gender strategies and sex ratios. The studies reviewed and the new results presented emphasize the role that shifts in the ecological and genetic context of plant populations may play in causing transitions between sexual systems.

Extremely reduced dispersal and gene flow in an island bird

The Réunion grey white-eye, Zosterops borbonicus, a passerine bird endemic to Réunion Island in the Mascarene archipelago, represents an extreme case of microgeographical plumage colour variation in birds, with four distinct colour forms occupying different parts of this small island (2512 km2). To understand whether such population differentiation may reflect low levels of dispersal and gene flow at a very small spatial scale, we examined population structure and gene flow by analysing variation at 11 microsatellite loci among four geographically close localities (<26 km apart) sampled within the distribution range of one of the colour forms, the brown-headed brown form. Our results revealed levels of genetic differentiation that are exceptionally high for birds at such a small spatial scale. This strong population structure appears to reflect low levels of historical and contemporary gene flow among populations, unless very close geographically (<10 km). Thus, we suggest that the Réunion grey white-eye shows an extremely reduced propensity to disperse, which is likely to be related to behavioural processes.

The role of selection and historical factors in driving population differentiation along an elevational gradient in an island bird

Adaptation to local environmental conditions and the range dynamics of populations can influence evolutionary divergence along environmental gradients. Thus, it is important to investigate patterns of both phenotypic and genetic variations among populations to reveal the respective roles of these two types of factors in driving population differentiation. Here, we test for evidence of phenotypic and genetic structure across populations of a passerine bird (Zosterops borbonicus) distributed along a steep elevational gradient on the island of Réunion. Using 11 microsatellite loci screened in 401 individuals from 18 localities distributed along the gradient, we found that genetic differentiation occurred at two spatial levels: (i) between two main population groups corresponding to highland and lowland areas, respectively, and (ii) within each of these two groups. In contrast, several morphological traits varied gradually along the gradient. Comparison of neutral genetic differentiation (FST) and phenotypic differentiation (PST) showed that PST largely exceeds FST at several morphological traits, which is consistent with a role for local adaptation in driving morphological divergence along the gradient. Overall, our results revealed an area of secondary contact midway up the gradient between two major, cryptic, population groups likely diverged in allopatry. Remarkably, local adaptation has shaped phenotypic differentiation irrespective of population history, resulting in different patterns of variation along the elevational gradient. Our findings underscore the importance of understanding both historical and selective factors when trying to explain variation along environmental gradients.

The Missing Response to Selection in the Wild

Although there are many examples of contemporary directional selection, evidence for responses to selection that match predictions are often missing in quantitative genetic studies of wild populations. This is despite the presence of genetic variation and selection pressures – theoretical prerequisites for the response to selection. This conundrum can be explained by statistical issues with accurate parameter estimation, and by biological mechanisms that interfere with the response to selection. These biological mechanisms can accelerate or constrain this response. These mechanisms are generally studied independently but might act simultaneously. We therefore integrated these mechanisms to explore their potential combined effect. This has implications for explaining the apparent evolutionary stasis of wild populations and the conservation of wildlife.

A practical guide to quantifying the effect of genes underlying adaptation in a mixed genomics and evolutionary ecology approach

Abstract In adaptation studies, approaches in genomics investigate the genetic, cellular and biochemical mechanisms involved in adaptation using model organisms. In study systems such as Arabidopsis, the demand is high to test for the effect of genes which polymorphism is known on the ability of plants to cope with adverse environmental conditions. In evolutionary ecology, understanding how selection and environmental heterogeneity shape the diversity of organisms is crucial. In that regard, tools to decipher how the architecture of standing genetic variation affects the evolutionary potential of plants to adapt are required. Quantitative genetics provide a range of statistical methods that could be used to study those questions but are generally neglected as a consequence of their scary name, as for example for the pedigree based random regression method used in our approach. Here, we provide a practical guide for researchers from multiple domains who would like to use such methods. We begin by providing an overview of some of the challenges in plant sciences, such as understanding the role of regulatory genes in adaptation that could gain from using such approach. We then illustrate the “how to” of the method by applying it to an imaginary example. We also provide a complete tutorial in the supplementary online material under the form of a protocol and data that can be used to train researchers and students by replicating entirely our approach. We conclude by highlighting the advantages and limits of such approach.

Genetic links among individuals: from genealogies to molecular markers

Abstract Genetic links among individuals are widely used to characterize the diversity of domesticated and natural populations and they also provide complementary information for statistical population summaries. We first discuss the measures used by geneticists based on genealogy and DNA data. The choice of metrics of genetic links should be coherent with the objectives: biodiversity or genotype–phenotype relationships. For the last objective, we evaluate by simulation the interest of genetic distances when the objective is the prediction of individual genetic values and phenotypes using kernel regression. A pseudo-distance based on correlations between marker genotypes of pairs of individual yields better predictions than other classical definition of distances.

Evolution without standing genetic variation: change in transgenerational plastic response under persistent predation pressure

Transgenerational phenotypic plasticity is a fast non-genetic response to environmental modifications that can buffer the effects of environmental stresses on populations. However, little is known about the evolution of plasticity in the absence of standing genetic variation although several non-genetic inheritance mechanisms have now been identified. Here we monitored the pea aphid transgenerational phenotypic response to ladybird predators (production of winged offspring) during 27 generations of experimental evolution in the absence of initial genetic variation (clonal multiplication starting from a single individual). We found that the frequency of winged aphids first increased rapidly in response to predators and then remained stable over 25 generations, implying a stable phenotypic reconstruction at each generation. We also found that the high frequency of winged aphids persisted for one generation after removing predators. Winged aphid frequency then entered a refractory phase during which it dropped below the level of control lines for at least two generations before returning to it. Interestingly, the persistence of the winged phenotype decreased and the refractory phase lasted longer with the increasing number of generations of exposure to predators. Finally, we found that aphids continuously exposed to predators for 22 generations evolved a significantly weaker plastic response than aphids never exposed to predators, which, in turn, increased their fitness in presence of predators. Our findings therefore showcased an example of experimental evolution of plasticity in the absence of initial genetic variation and highlight the importance of integrating several components of non-genetic inheritance to detect evolutionary responses to environmental changes.