Rafael Rubio de Casas

Current perspectives and the future of domestication studies

It is difficult to overstate the cultural and biological impacts that the domestication of plants and animals has had on our species. Fundamental questions regarding where, when, and how many times domestication took place have been of primary interest within a wide range of academic disciplines. Within the last two decades, the advent of new archaeological and genetic techniques has revolutionized our understanding of the pattern and process of domestication and agricultural origins that led to our modern way of life. In the spring of 2011, 25 scholars with a central interest in domestication representing the fields of genetics, archaeobotany, zooarchaeology, geoarchaeology, and archaeology met at the National Evolutionary Synthesis Center to discuss recent domestication research progress and identify challenges for the future. In this introduction to the resulting Special Feature, we present the state of the art in the field by discussing what is known about the spatial and temporal patterns of domestication, and controversies surrounding the speed, intentionality, and evolutionary aspects of the domestication process. We then highlight three key challenges for future research. We conclude by arguing that although recent progress has been impressive, the next decade will yield even more substantial insights not only into how domestication took place, but also when and where it did, and where and why it did not.

The scope of Baker's law

Bakers law refers to the tendency for species that establish on islands by long-distance dispersal to show an increased capacity for self-fertilization because of the advantage of self-compatibility when colonizing new habitat. Despite its intuitive appeal and broad empirical support, it has received substantial criticism over the years since it was proclaimed in the 1950s, not least because it seemed to be contradicted by the high frequency of dioecy on islands. Recent theoretical work has again questioned the generality and scope of Bakers law. Here, we attempt to discern where the idea is useful to apply and where it is not. We conclude that several of the perceived problems with Bakers law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Bakers law should be read in terms of an enrichment of a capacity for uniparental reproduction in colonizing situations, rather than of high selfing rates. We suggest that Bakers law might be tested in four different contexts, which set the breadth of its scope: the colonization of oceanic islands, metapopulation dynamics with recurrent colonization, range expansions with recurrent colonization, and colonization through species invasions.

Pleiotropy in the wild: the dormancy gene DOG1 exerts cascading control on life cycles.

In the wild, organismal life cycles occur within seasonal cycles, so shifts in the timing of developmental transitions can alter the seasonal environment experienced subsequently. Effects of genes that control the timing of prior developmental events can therefore be magnified in the wild because they determine seasonal conditions experienced by subsequent life stages, which can influence subsequent phenotypic expression. We examined such environmentally induced pleiotropy of developmental‐timing genes in a field experiment with Arabidopsis thaliana. When studied in the field under natural seasonal variation, an A. thaliana seed‐dormancy gene, Delay Of Germination 1 (DOG1), was found to influence not only germination, but also flowering time, overall life history, and fitness. Flowering time of the previous generation, in turn, imposed maternal effects that altered germination, the effects of DOG1 alleles, and the direction of natural selection on these alleles. Thus under natural conditions, germination genes act as flowering genes and potentially vice versa. These results illustrate how seasonal environmental variation can alter pleiotropic effects of developmental‐timing genes, such that effects of genes that regulate prior life stages ramify to influence subsequent life stages. In this case, one gene acting at the seed stage impacted the entire life cycle.

Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach

UNLABELLED PREMISE OF THE STUDY We sought novel evolutionary insights for the highly diverse Saxifragales by constructing a large phylogenetic tree encompassing 36.8% of the species-level biodiversity. • METHODS We built a phylogenetic tree for 909 species of Saxifragales and used this hypothesis to examine character evolution for annual or perennial habit, woody or herbaceous habit, ovary position, petal number, carpel number, and stamen to petal ratio. We employed likelihood approaches to investigate the effect of habit and life history on speciation and extinction within this clade. • KEY RESULTS Two major shifts occurred from a woody ancestor to the herbaceous habit, with multiple secondary changes from herbaceous to woody. Transitions among superior, subinferior, and inferior ovaries appear equiprobable. A major increase in petal number is correlated with a large increase in carpel number; these increases have co-occurred multiple times in Crassulaceae. Perennial or woody lineages have higher rates of speciation than annual or herbaceous ones, but higher probabilities of extinction offset these differences. Hence, net diversification rates are highest for annual, herbaceous lineages and lowest for woody perennials. The shift from annuality to perenniality in herbaceous taxa is frequent. Conversely, woody perennial lineages to woody annual transitions are infrequent; if they occur, the woody annual state is left immediately. • CONCLUSIONS The large tree provides new insights into character evolution that are not obvious with smaller trees. Our results indicate that in some cases the evolution of angiosperms might be conditioned by constraints that have been so far overlooked.

Storytelling and story testing in domestication

Significance Our knowledge of the domestication of animal and plant species comes from a diverse range of disciplines, and interpretation of patterns in data from these disciplines has been the dominant paradigm in domestication research. However, such interpretations are easily steered by subjective biases that typically fail to account for the inherent randomness of evolutionary processes, and which can be blind to emergent patterns in data. The testing of explicit models using computer simulations, and the availability of powerful statistical techniques to fit models to observed data, provide a scientifically robust means of addressing these problems. Here we outline the principles and argue for the merits of such approaches in the context of domestication-related questions. The domestication of plants and animals marks one of the most significant transitions in human, and indeed global, history. Traditionally, study of the domestication process was the exclusive domain of archaeologists and agricultural scientists; today it is an increasingly multidisciplinary enterprise that has come to involve the skills of evolutionary biologists and geneticists. Although the application of new information sources and methodologies has dramatically transformed our ability to study and understand domestication, it has also generated increasingly large and complex datasets, the interpretation of which is not straightforward. In particular, challenges of equifinality, evolutionary variance, and emergence of unexpected or counter-intuitive patterns all face researchers attempting to infer past processes directly from patterns in data. We argue that explicit modeling approaches, drawing upon emerging methodologies in statistics and population genetics, provide a powerful means of addressing these limitations. Modeling also offers an approach to analyzing datasets that avoids conclusions steered by implicit biases, and makes possible the formal integration of different data types. Here we outline some of the modeling approaches most relevant to current problems in domestication research, and demonstrate the ways in which simulation modeling is beginning to reshape our understanding of the domestication process.

The Correlated Evolution of Dispersal and Mating-System Traits

The existence of an evolutionary syndrome linking dispersal and mating-system traits has been discussed in both plants and animals. In animals, dispersal as a means of inbreeding-avoidance has been cited as an ultimate cause of sex-biased dispersal. In plants, self-compatibility is widespread, which is often cited as a mechanism for reproductive assurance in organisms that have limited control of dispersal. Limited dispersal has also been hypothesized to minimize outbreeding depression and increase local adaptation. Here, we compare and contrast the various evolutionary hypotheses that link dispersal and the mating system in both plants and animals. We conclude that the majority of theoretical evidence supports the existence of two evolutionary syndromes: (1) outcrossing and dispersing; (2) inbreeding and not dispersing. In the light of the evidence compiled, we advocate for a redefinition of Baker’s law, which we consider to be an exception rather than the rule. As environmental heterogeneity is common in nature, the role of bet-hedging in the evolution of these strategies is likely to be very strong, albeit difficult to prove empirically. Lastly, we argue that exceptions to these two general syndromes (e.g., inbreeding and dispersing) should not be viewed as contradictory; instead they merit exceptional attention because they represent unusual biological adaptations. Throughout, we refer to specific empirical examples to illustrate these scenarios and conclude by suggesting that a meta-analysis of the available data would be a useful next step.

Phenotypic plasticity and integration across the canopy of Olea europaea subsp. guanchica (Oleaceae) in populations with different wind exposures.

Woody plants, as sessile and long-lived organisms, are expected to have effective mechanisms for dealing with recurrent environmental stresses. In the present study, we hypothesized that phenotypic plasticity (the ability to express alternative phenotypes) and integration (covariation among functionally related traits) are elicited in plants under stressful wind speed conditions. We investigated the within-crown variation of nine vegetative traits of a tree species (Olea europaea subsp. guanchica) in six populations that represented a gradient of wind speed exposures. Wind-exposed twigs in outer-canopy layers had smaller leaves; thinner, lighter, and shorter internodes; and a larger internode cross-sectional area to leaf area ratio. Comparison between field and greenhouse trials revealed that field differences among populations were mediated by phenotypic plasticity. Outer-canopy twigs expressed plastic responses in populations exposed to high wind speeds, whereas inner-canopy twigs displayed high phenotypic convergence among populations. In addition, phenotypic integration increased with wind exposure (outer canopy > inner canopy > greenhouse) and was consequently affected by canopy openness. We conclude that exposure to wind above a certain speed threshold in this woody species elicits a plastic response that is associated with increased integration among traits and involves mechanical and hydraulic rearrangements in more exposed parts of the trees.

Gene-flow through space and time: dispersal, dormancy and adaptation to changing environments

Dispersal through space or time (via dormancy) determines gene flow and influences demography. Because of their functional similarities, a covariation between dispersal and dormancy is expected. Dispersal and dormancy are anatomically linked in plants, because they both depend on attributes of the seed, albeit this anatomical association is rarely considered when analyzing interactions between dispersal and dormancy. In this paper, we investigate the extent to which dispersal and dormancy can be expected to correlate and how each might influence adaptation to novel environments such as those brought on by climate change. We review the theoretical and empirical literature on the subject with a focus on seed plants. We find that although a negative correlation between dispersal and dormancy has been theoretically anticipated, several models predict deviations from this expectation under scenarios of environmental heterogeneity. The empirical evidence does not support any specific covariation pattern, likely because the interaction between dispersal and dormancy is affected by multiple environmental and developmental constraints. From a climate change perspective, the effects of dispersal and dormancy on population structure are not equivalent: dormancy-mediated gene flow is intrinsically asymmetric (from the past towards the future) whereas spatial dispersal is not necessarily directional. As a result, selection on traits linked to dormancy and dispersal might differ qualitatively. In particular, gene flow through dormancy can only be adaptive if future environmental conditions are similar to those of the past, or if it contributes to novel allelic combinations. We conclude that, in spite of a long tradition of research, we are unable to anticipate a universal relationship between dispersal and dormancy. More work is needed to predict the relative contributions of spatial dispersal and dormancy to gene flow and adaptation to novel environments.

Diversification and the evolution of dispersal ability in the tribe Brassiceae (Brassicaceae)

BACKGROUND AND AIMS Dispersal and establishment ability can influence evolutionary processes such as geographic isolation, adaptive divergence and extinction probability. Through these population-level dynamics, dispersal ability may also influence macro-evolutionary processes such as species distributions and diversification. This study examined patterns of evolution of dispersal-related fruit traits, and how the evolution of these traits is correlated with shifts in geographic range size, habitat and diversification rates in the tribe Brassiceae (Brassicaceae). METHODS The phylogenetic analysis included 72 taxa sampled from across the Brassiceae and included both nuclear and chloroplast markers. Dispersal-related fruit characters were scored and climate information for each taxon was retrieved from a database. Correlations between fruit traits, seed characters, habitat, range and climate were determined, together with trait-dependent diversification rates. KEY RESULTS It was found that the evolution of traits associated with limited dispersal evolved only in association with compensatory traits that increase dispersal ability. The evolution of increased dispersal ability occurred in multiple ways through the correlated evolution of different combinations of fruit traits. The evolution of traits that increase dispersal ability was in turn associated with larger seed size, increased geographic range size and higher diversification rates. CONCLUSIONS This study provides evidence that the evolution of increased dispersal ability and larger seed size, which may increase establishment ability, can also influence macro-evolutionary processes, possibly by increasing the propensity for long-distance dispersal. In particular, it may increase speciation and consequent diversification rates by increasing the likelihood of geographic and thereby reproductive isolation.

Variation in sclerophylly among Iberian populations of Quercus coccifera L. is associated with genetic differentiation across contrasting environments

Evergreen oaks are an emblematic element of the Mediterranean vegetation and have a leaf phenotype that seems to have remained unchanged since the Miocene. We hypothesise that variation of the sclerophyll phenotype among Iberian populations of Quercus coccifera is partly due to an ulterior process of ecotypic differentiation. We analysed the genetic structure of nine Iberian populations using ISSR fingerprints, and their leaf phenotypes using mean and intracanopy plasticity values of eight morphological (leaf angle, area, spinescence, lobation and specific area) and biochemical traits (VAZ pool, chlorophyll and beta-carotene content). Climate and soil were also characterised at the population sites. Significant genetic and phenotypic differences were found among populations and between NE Iberia and the rest of the populations of the peninsula. Mean phenotypes showed a strong and independent correlation with both genetic and geographic distances. Northeastern plants were smaller, less plastic, with smaller, spinier and thicker leaves, a phenotype consistent with the stressful conditions that prevailed in the steppe environments of the refugia within this geographic area during glaciations. These genetic, phenotypic, geographic and environmental patterns are consistent with previously reported palaeoecological and common evidence. Such consistency leads us to conclude that there has been a Quaternary divergence within the sclerophyllous syndrome that was at least partially driven by ecological factors.