Exaptation Traits for Megafaunal Mutualisms as a Factor in Plant Domestication

Abstract

Megafaunal extinctions are recurring events that cause evolutionary ripples, as cascades of secondary extinctions and shifting selective pressures reshape ecosystems. Megafaunal browsers and grazers are major ecosystem engineers, they: keep woody vegetation suppressed; are nitrogen cyclers; and serve as seed dispersers. Most angiosperms possess sets of physiological traits that allow for the fixation of mutualisms with megafauna; some of these traits appear to serve as exaptation (preadaptation) features for farming. As an easily recognized example, fleshy fruits are, an exaptation to agriculture, as they evolved to recruit a non-human disperser. We hypothesize that the traits of rapid annual growth, self-compatibility, heavy investment in reproduction, high plasticity (wide reaction norms), and rapid evolvability were part of an adaptive syndrome for megafaunal seed dispersal. We review the evolutionary importance that megafauna had for crop and weed progenitors and discuss possible ramifications of their extinction on: (1) seed dispersal; (2) population dynamics; and (3) habitat loss. Humans replaced some of the ecological services that had been lost as a result of late Quaternary extinctions and drove rapid evolutionary change resulting in domestication.

Keywords: crops; domestication; ecosystem engineering; endozoochory; exaptation; megafauna; origins of agriculture; seed dispersal.

Figure 1

Map showing centers or regions of crop domestication. Each color corresponds to a different millennium, specifically indicating when the earliest trait of domestication was fully introgressed into the crop population for that center, a full chronology of these domestications is presented in Table 1. Only crops with a clear archaeobotanical signal for domestication are presented hear and the least controversial dates are presented. This map intentionally does not account for any concept of pristine or secondary centers.

Figure 2

From top left: (1) Photo of horses consuming wild apples in the Tien Shan apple forests of Kazakhstan, photo taken by Artur Stroscherer and Martin Stuchtey. (2) Yaks grazing in Tibet have significant ecological impacts, photo by lead author. (3) Giraffes near the Olduvai Camp in Tanzania browsing on Acacia trees, photo taken by Yiming Wang. (4) Bison in Missouri on a heavily grazed field of herbaceous annuals, most of which are well adapted to heavy herbivory and disturbed ecosystems, photo by lead author.

Figure 3

A timeline showing key coevolutionary processes that created mutualistic relationships between large mammals and crop and weed progenitors. A deep time look at domestication helps lay the foundation for understanding evolution under cultivation. Elephantine dental structure depictions from Ferretti (2008) and horse teeth provided by William Taylor.