The evolutionary fate of phenotypic plasticity and functional traits under domestication in manioc: changes in stem biomechanics and the appearance of stem brittleness

PLoS One. 2013 Sep 4;8(9):e74727. doi: 10.1371/journal.pone.0074727. eCollection 2013.

Abstract

Domestication can influence many functional traits in plants, from overall life-history and growth form to wood density and cell wall ultrastructure. Such changes can increase fitness of the domesticate in agricultural environments but may negatively affect survival in the wild. We studied effects of domestication on stem biomechanics in manioc by comparing domesticated and ancestral wild taxa from two different regions of greater Amazonia. We compared mechanical properties, tissue organisation and wood characteristics including microfibril angles in both wild and domesticated plants, each growing in two different habitats (forest or savannah) and varying in growth form (shrub or liana). Wild taxa grew as shrubs in open savannah but as lianas in overgrown and forested habitats. Growth form plasticity was retained in domesticated manioc. However, stems of the domesticate showed brittle failure. Wild plants differed in mechanical architecture between shrub and liana phenotypes, a difference that diminished between shrubs and lianas of the domesticate. Stems of wild plants were generally stiffer, failed at higher bending stresses and were less prone to brittle fracture compared with shrub and liana phenotypes of the domesticate. Biomechanical differences between stems of wild and domesticated plants were mainly due to changes in wood density and cellulose microfibril angle rather than changes in secondary growth or tissue geometry. Domestication did not significantly modify "large-scale" trait development or growth form plasticity, since both wild and domesticated manioc can develop as shrubs or lianas. However, "finer-scale" developmental traits crucial to mechanical stability and thus ecological success of the plant were significantly modified. This profoundly influenced the likelihood of brittle failure, particularly in long climbing stems, thereby also influencing the survival of the domesticate in natural situations vulnerable to mechanical perturbation. We discuss the different selective pressures that could explain evolutionary modifications of stem biomechanical properties under domestication in manioc.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biomechanical Phenomena
  • Ecosystem
  • Elasticity*
  • Evolution, Molecular*
  • Manihot / growth & development
  • Manihot / physiology*
  • Phenotype*
  • Plant Stems / physiology*
  • Stress, Mechanical

Grants and funding

This research was funded by the following grants: 1) Contrats Projets Etat Région (CPER) Guyane to DM. www.datar.gouv.fr/contrats-etat-regions. 2) Programme ‘Ecosystèmes Tropicaux’ from the French Ministry of Ecology and Sustainable Development, to study the diversity of Manihot in French Guiana to DM. http://www.agropolis.fr/actualites/retour-seminaire-ecosystemes-tropicaux-ecofor-2010.php. 3) Programme of the French National Research Agency (ANR-05-BDIV-012-04) to N. Rowe and B. Clair. www.agence-nationale-recherche.fr. 4) This work also benefited from an "Investissement d’Avenir" grant managed by the Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01). www.labex-ceba.fr. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.