The Evolutionary Fate of Phenotypic Plasticity and Functional Traits under Domestication in Manioc: Changes in Stem Biomechanics and the Appearance of Stem Brittleness

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 bot

Maximum bending stress (MPa) against proportion of wood to axial second moment of area of the stem.

<p>(A) Shrub phenotypes of the wild taxon show higher values of maximum stress compared with shrub phenotypes of the domesticate. (B) Climber phenotypes of wild and domesticated taxa show little difference in maximum bending stress.</p

Wild and domesticated manioc from French Guiana: Spearman rank correlation coefficients (R_s) of wood cylinder geometry (% contribution of wood cylinder to axial second moment of area of stem) with (i) Young’s modulus (bending) and (ii) maximum bending stress.

<p>Wild and domesticated manioc from French Guiana: Spearman rank correlation coefficients (R_s) of wood cylinder geometry (% contribution of wood cylinder to axial second moment of area of stem) with (i) Young’s modulus (bending) and (ii) maximum bending stress.</p

Stiffness (MPa) against proportion of wood cylinder to second moment of area of the stem.

<p>(A) Shrub phenotypes of the wild taxon show significantly higher stem stiffness for a given contribution of wood cylinder to second moment of area compared with shrubs of the domesticate. (B) A similar, but less marked difference is seen between climber phenotypes of the wild and domesticated taxa.</p

Vessel size and density traits (means ± s. d.) with <i>P</i>-values of Mann–Whitney tests comparing medians between shrub phenotypes of the wild and domesticated manioc and between climber phenotypes of these two taxa.

<p>Vessel size and density traits (means ± s. d.) with <i>P</i>-values of Mann–Whitney tests comparing medians between shrub phenotypes of the wild and domesticated manioc and between climber phenotypes of these two taxa.</p

Microfibril angle for shrub and climber phenotypes of wild and domesticated manioc in French Guiana.

<p>(A) MFA at relative distances within wood cylinder from pith to bark for wild and domesticated shrubs. (B) MFA at relative distance within wood cylinder from pith to bark for shrubs and climbers of the domesticate. (C) Young’s modulus against MFA at periphery of wood cylinder for shrub phenotypes of the wild and the domesticated taxon. Each symbol represents a segment of stem in the range of 0.3 to 2.5 m above ground level. (D) Young’s modulus against MFA at periphery of wood cylinder for shrubs and climbers of the domesticate. Each symbol represents a segment of stem in the range of 0.3 to 4.0 m above ground level.</p

Xylem tissue traits as measured in transverse sections (means ± s. d.) with <i>P</i>-values of Mann–Whitney tests comparing medians between shrub phenotypes of wild and domesticated manioc and between climber phenotypes of these two taxa in French Guiana.

<p>Xylem tissue traits as measured in transverse sections (means ± s. d.) with <i>P</i>-values of Mann–Whitney tests comparing medians between shrub phenotypes of wild and domesticated manioc and between climber phenotypes of these two taxa in French Guiana.</p

Box plots of maximum stress for shrub and climber phenotypes of wild and domesticated manioc.

<p>(A) Wild shrubs from French Guiana show consistently higher values of maximum stress compared with wild climbers. (B) There is no difference in maximum stress between shrubs and climbers in the domesticated species from French Guiana. (Graph and statistics parameters as for Fig. 3; Mann-Whitney test not performed on size class 10.1–15.0 mm because of limited sample size).</p

Transverse sections of wood cylinders showing different starch grain densities from French Guiana.

<p>(A) Wild shrub (B) domesticated shrub Sections were made at a thickness of 60 µm and stained with 1% iodine solution in 90% ethanol for 5 minutes; scale bar  =  250 µm).</p

Box plots of Young’s modulus for shrub and climber phenotypes of wild and domesticated manioc.

<p>(A) Shrubs of the wild relative from French Guiana have stems comprised of consistently stiffer materials than climbing stems in all size classes. (B) Stems of domesticated <i>M. esculenta</i> from French Guiana are generally less stiff than those of the wild taxon and there is a less consistent difference in stiffness between shrubs and climbers in the domesticate. Sample sizes (box plots: medians, 1^st, 3^rd interquartiles, outliers [>1.5 x IQR above 3^rd quartile or below 1^st quartile] and extreme values [>3 x IQR above 3^rd quartile or below 1^st quartile]; probability values refer to Mann-Whitney comparisons of median values).</p