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Early human selection of crops’ wild progenitors explains the acquisitive physiology of modern cultivars

Nature Plants volume 10, pages 25–36 (2024)Cite this article

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Abstract

Crops have resource-acquisitive leaf traits, which are usually attributed to the process of domestication. However, early choices of wild plants amenable for domestication may also have played a key role in the evolution of crops’ physiological traits. Here we compiled data on 1,034 annual herbs to place the ecophysiological traits of 69 crops’ wild progenitors in the context of global botanical variation, and we conducted a common-garden experiment to measure the effects of domestication on crop ecophysiology. Our study found that crops’ wild progenitors already had high leaf nitrogen, photosynthesis, conductance and transpiration and soft leaves. After domestication, ecophysiological traits varied little and in idiosyncratic ways. Crops did not surpass the trait boundaries of wild species. Overall, the resource-acquisitive strategy of crops is largely due to the inheritance from their wild progenitors rather than to further breeding improvements. Our study concurs with recent literature highlighting constraints of crop breeding for faster ecophysiological traits.

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Fig. 1: Conceptual framework.
Fig. 2: Early human selection.
Fig. 3: Evolution under cultivation.
Fig. 4: Domesticates versus wilds.

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Data availability

Most of the data used to compile the global dataset are publicly available in plant databases (the TRY plant trait database (www.try-db.org), the Botanical Information and Ecology Network database (https://bien.nceas.ucsb.edu/bien/), the AusTraits database (www.austraits.org), the China Plant Trait database (https://doi.org/10.1038/s41597-022-01884-4), the LEDA traitbase (www.leda-traitbase.org), the Plants of the World Online database (www.plantsoftheworldonline.org), and Crop Origins database (https://github.com/rubenmilla/Crop_Origins_Phylo/) and in published literature (Supplementary Table 1). The raw data of the experimental dataset and compiled species-level data on woodiness, growth form, life cycle and photosynthetic pathway are openly available at https://doi.org/10.6084/m9.figshare.24312577.v2 (ref. 106).

Code availability

The analyses carried out in this paper did not require the development of custom code. Functions were run as provided by the R packages mentioned in Methods.

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Acknowledgements

We thank A. Fernández for her help with plant sampling, M. Ramos and M. Blanco-Sánchez for their assistance with stable isotope analyses, and P. A. Martínez and M. S. Przybylska for statistical advice on phylogenetic and hypervolume analyses, respectively. This research was funded by an AEET Young Researchers grant to A.G.-F., by projects nos. CGL2017-83855-R and PID2021-122296NB-I00 (MINECO, Spain) to R.M. and by project no. REMEDINAL3-CM/S2013/MAE-2719 to I.A. A.G.-F. was supported by CAM (no. PEJD-2017-PRE/AMB-3598) and URJC (no. PREDOC20-030-1545) predoctoral fellowships and an Erasmus+ short mobility grant.

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Authors and Affiliations

  1. Grupo de investigación en Ecología Evolutiva, Departamento de Biología y Geología, Física y Química Inorgánica, Instituto de Investigación en Cambio Global, Universidad Rey Juan Carlos, Madrid, Spain

    Alicia Gómez-Fernández & Rubén Milla

  2. Instituto de Ciencias Forestales, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Consejo Superior de Investigaciones Científicas, Madrid, Spain

    Ismael Aranda

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  1. Alicia Gómez-Fernández
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A.G.-F. compiled and analysed the data, interpreted the results and prepared the draft paper. All authors contributed to the study conception and design, collected the experimental data, and reviewed and approved the final version of the paper.

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Correspondence to Alicia Gómez-Fernández or Rubén Milla.

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Nature Plants thanks Jaume Flexas, Eric von Wettberg and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Univariate comparisons between domesticates and wild species that were never domesticated in the ecophysiological traits.

Domesticates (D) are shown in orange and wild annual herbs (W) in green. Symbols indicate photosynthetic pathway: C3 (circles) versus C4 (triangles). Points are trait mean of species grouped by botanical order. Statistical differences were evaluated from phylogenetic generalized least squares (PGLS) models across 1000 randomly resolved trees and asterisks denote the mean P value based on analysis of variance (ANOVA) tests (., P < 0.1; *, P < 0.05; **, P < 0.01; ***, P < 0.001). Total sample size is shown for each trait, plant type (D, W) and photosynthetic pathway. Abbreviations: Aarea, net photosynthetic rate per unit area; gwv, stomatal conductance to water vapour; [Nmass], mass-based leaf N concentration; SLA, specific leaf area; and δ13C, 13C isotopic composition.

Extended Data Fig. 2 Trait correlations.

Correlations among log10-transformed ecophysiological traits plotted separately for photosynthetic pathway (C3, C4). Solid lines represent the fitted phylogenetic generalised least squares (PGLS) model and were drawn when trait correlation was significant (P < 0.05). PGLSs included one ecophysiological trait as response variable and the interaction between another ecophysiological trait and photosynthetic pathway as fixed effects. Abbreviations: Aarea, net photosynthetic rate per unit area; gwv, stomatal conductance to water vapour; [Nmass], mass-based leaf N concentration; SLA, specific leaf area; and δ13C, 13C isotopic composition.

Extended Data Fig. 3 Organ under selection.

Ecophysiological traits between the different types of crops’ wild progenitors depending on the organ under selection (either fruit/flower, leaf/shoot, or seed). Wild species that were never domesticated were included in the plot (*None). Dots are trait mean of species. Boxplots show the median and 25th and 75th percentiles of the data, with whiskers extending to 1.5 times the interquartile range. Models were tested with phylogenetic generalized least squares (PGLS). Different letters indicate significant differences among types of crops’ wild progenitors at P < 0.05, after multiple comparisons tests with false-discovery rate correction. Abbreviations: Aarea, net photosynthetic rate per unit area; gwv, stomatal conductance to water vapour; [Nmass], mass-based leaf N concentration; SLA, specific leaf area; and δ13C, 13C isotopic composition. For SLA, one wild progenitor selected for its roots was removed from the multiple comparisons tests because there was no other data belonging to this category.

Extended Data Fig. 4 Effect sizes of domestication and improvement.

Effect sizes of domestication (landrace-progenitor comparisons) and improvement (improved-landrace comparisons) on the five studied ecophysiological traits: net photosynthetic rate per unit area (a), stomatal conductance to water vapour (b), mass-based leaf N concentration (c), specific leaf area (d), and 13C isotopic composition (e), for each crop included in the experimental dataset. The dots are the effect sizes estimated by Hedges´G and the bars are the 95% confidence intervals. Hedges’ G was computed as the difference in means between landraces and wild progenitors (domestication effect size; n = 16 for each crop) or improved cultivars and landraces (improvement effect size; n = 16 for each crop) divided by the pooled and weighted standard deviation of the two groups. Negative scores of Hedges’ G indicate negative effects of domestication or improvement on the ecophysiological traits.

Extended Data Fig. 5 Results of principal components analysis for mass-based leaf N concentration ([Nmass]) and 13C isotopic composition (δ13C).

Ellipses represent 95% confidence areas for domesticates (orange) and wild species (green). Centroids are represented by the largest point of the same colour, while the smaller points represent individual species. Axes percentages represent the amount of variation accounted for by each principal component.

Extended Data Table 1 Range of variation in leaf ecophysiological traits and summary of data compilation
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Extended Data Table 2 Results of phylogenetic generalised least squares models (PGLSs) examining the effects of early selection on ecophysiological traits for (a) the global dataset and for (b) indoor experiments
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Extended Data Table 3 Results of phylogenetic generalised least squares models (PGLSs) examining the effects of early selection on ecophysiological traits for (a) cereals, (b) legumes, and (c) forbs
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Extended Data Table 4 Results of linear mixed-effects models (LMMs) testing the effects of domestication and improvement on ecophysiological traits
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Extended Data Table 5 Results of hypervolume analyses
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Gómez-Fernández, A., Aranda, I. & Milla, R. Early human selection of crops’ wild progenitors explains the acquisitive physiology of modern cultivars. Nat. Plants 10, 25–36 (2024). https://doi.org/10.1038/s41477-023-01588-6

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