The fruits of our labour: the evolution of crops

#Guest post by Francesco Janzen.

Have you ever wondered how much work and time has been put into producing the food you eat today: that juicy apple, or that fresh loaf of bread? In modern times, we can easily recognize fruits and vegetables such as tomatoes, corn, and bananas, but would it surprise you that these foods have not always looked the way they do? Like all parts of the living world, food crops have changed much over time, and this change is directly linked to human efforts (Purseglove, 1965; Allaby et al., 2015). 

Agriculture began approximately 11,000-12,000 years ago, and has originated in several parts of the world (National Geographic, 2015). Humans domesticated wheat in the Fertile Crescent, or Near East approximately 8,000-9,000 years ago. (Nevo, 2014; National Geographic, 2015). In China, rice is proposed to have been domesticated 10,000-20,000 years ago (Gross & Zhao, 2014; National Geographic, 2015). Across the ocean, squash was domesticated about 10,000 years ago in what is known today as Mexico, and the beginning of sunflower cultivation began in North America around 5,000 years ago (Janick, 2013; National Geographic, 2015). All of these domestications began with wild progenitors of today’s crop species (Gross et al., 2014; Allaby et al., 2015).  

But how did the wild crops of ancient times develop into the modern ones we know today? John William Purseglove, a former tropical agricultural officer and director of the Singapore Botanic Gardens, discussed the ways in which humans have changed crop species over time in a chapter of “The Genetics of Colonizing Species” (1965). In his chapter, “The Spread of Tropical Crops”, Purseglove (1965) states that humans would have begun the first agricultural crops with a subset of desired plants from the original wild population. This subset would not possess the genetic diversity of the original population, essentially producing a genetic bottleneck effect (Purseglove, 1965). Furthermore, certain desired traits would be selected for in this new population, so breeding strategies would overtime change the traits expressed, such as larger fruit, seedless fruit, lack of defense mechanisms, etc. (Purseglove, 1965). Although they benefit humans, these changes could potentially decrease the competitive ability of these new plants. This intrinsically ties their survival to human assistance (Purseglove, 1965). 

Humans have not only changed the physical characteristics of crop plants; they have altered their geographic distributions as well. Compared to their wild ancestors, most crop plants are now grown in areas far removed from their origin, such as with vanilla (Vanilla planifolia). Vanilla originated in Mexico, but is now grown in large numbers in Madagascar (Purseglove, 1965). In fact, vanilla and most other crops are much more successful in their new environments, but why is this so? Purseglove (1965) proposed that by moving a crop plant into a new habitat where predators or disease are absent, little would control population sizes, and increase crop yields. 

Visible difference between a wild strawberry (Fragaria virginiana, left) and a domestic strawberry (Fragaria x ananassa, right), from http://www.jamesandthegiantcorn.com/tag/domestication/. 

The new environments that domestic crops are exposed to may further increase the genetic gap with their wild ancestors. Under new, adverse environmental conditions, a population of a crop may be culled, save for a few individuals possessing recessive genes that confer a benefit to coping with the altered conditions (Purseglove, 1965). The remaining individuals reproduce, which shifts the next generation’s genotypic frequency (Purseglove, 1965). In addition, this can effectively expand the range of the domestic crop, whereas the wild type remains restricted to its original range (Purseglove, 1965). 

Science has come a long way since Purseglove proposed his ideas 50 years ago, and the advent of DNA has helped improve our understanding of evolution. With respect to the evolution of crops, DNA allows for testing of certain theories proposed, one such being the bottleneck effect. A study conducted by Gross et al. (2014) investigated whether perennial crop species, specifically the apple (Malus x domestica) showed a decrease in genetic diversity when compared to closely related wild species. They expected that there would have been a narrowing of genetic diversity at two moments in history. Firstly, during a domestication bottleneck, similar to that proposed by Purseglove (1965), and secondly during an improvement bottleneck, where desirable traits in the crop species were selected for to produce elite cultivars (Gross et al., 2014). 

A visual depiction of the bottleneck effect, where the bottleneck represents stochastic (random) events, from http://bio1151.nicerweb.com/Locked/media/ch23/bottleneck.html. 

By sequencing specific DNA regions of 11 varieties of apple cultivar (both ancient and modern), and that of three wild species, Gross et a. (2014) sought to demonstrate that domesticated cultivars show less genetic diversity than wild species. The regions selected were areas where each species show a variable amount of repeated sequence length, known as microsatellites, allowing for easy comparison of genetic quality (Gross et al., 2014). What they found, contrary to what was expected, was that domestic apples have not undergone a significant reduction of genetic diversity, either at the domestication or improvement phases (Gross et al., 2014). This evidence shows that not all theories produced 50 or more years ago withstand the test of time, especially when new tools to test these theories become available.   

So how does any of this information impact management practice of controlling invasive species? Purseglove (1965) stated in his chapter that by understanding the evolution of crop species, we gain insight into the success of introduced weed species. Although weeds do not require any human assistance in survival, the forces acting on them may be the similar to those acting on agricultural crops. Just as crops experience a release from predators and disease when removed from their native habitats, weeds may also undergo this release, contributing to their widespread success (Purseglove, 1965). This parallel could be quite useful in the understanding and management of weedy species.  

References: 

Allaby, R.G., Gutaker R., Clarke, A.C., Pearson, N., Ware, R., Palmer, S.A., Kitchen, 

J.L., and Smith, O. 2015. Using archaeogenomic and computational approaches to unravel the history of local adaptation in crops. Philosophical Transactions Royal Society  370: 20130377.

Gross, B.L., Henk, A.D., Richards, C.M., Fazio, G., and Volk, G.M. 2014. Genetic 

diversity in Malus × Domestica (Rosaceae) through time in response to domestication. American Journal of Botany 101(10): 1770-1779.   

Gross, B.L. & Zhao, Z. 2014. Archaeological and genetic insights into the origins of 

domesticated rice. Proceedings of the National Academy of Sciences 111(17): 6190-6197. 

Janick, J. 2013. Development of New World crops by indigenous Americans. 

Horticultural Science 48(4): 406-412.   

National Geographic Society. 2015. The development of agriculture. Retrieved from 

https://genographic.nationalgeographic.com/development-of-agriculture/. 

Nevo, E. 2014. Evolution of wild emmer wheat and crop improvement. Journal of 

Systematics and Evolution 52(6): 673-696. 

Purseglove, J.W. (1965). The spread of tropical crops. In H.G. Baker, and G.L Stebbins 

(Eds.). The Genetics of Colonizing Species. New York: Academic Press.

Waste not, want not? How human food waste changes ecosystems

Daniel Oro, Meritxell Genovart, Giacomo Tavecchia, Mike S. Fowler and Alejandro Martínez-Abraín. 2013. Ecological and evolutionary implications of food subsidies from humans. Ecology Letters. Volume 16, Issue 12, pp 1501–1514. DOI: 10.1111/ele.12187

Humans have always been connected to their environment, directly and indirectly. Ecologists in particular, and people in general, have been thinking about the causes and consequences of these connections for hundreds of years. One form of interaction results when human food resources become available to other animals – for example, through waste dumps, crop waste, fishery by-catches, bird feeders, or road kill. Starting with middens and waste piles in early human settlements, our food waste has always passed t

Garbage dump in India.

o other species. And while rarely considered compared to human impacts like habitat destruction and climate change, a new review by Daniel Oro and colleagues argues that these subsidies have shaped ecosystems around the globe.

Human food waste (aka subsidies) may come from a variety of human activities, with the three most prominent being crop residuals (remnants of harvest remaining on fields), waste dumps, and fishery discards (by-catch thrown overboard). Each of these forms of subsidy occurs globally and large numbers of species rely partially or completely on them for food. For example, dumps are global in distribution, and contain enough edible waste to attract 20-30% of all mammal and bird in a region (particularly omnivorous and carnivorous species). Crop residues usually attract herbivorous or granivorous species (particularly birds), while fisheries’ waste alter marine ecosystems. Eight percent of all catch (~7 million tonnes!) is simply released back into the ocean, and this supplements species across the food web, including half of all seabirds.

Food waste from human activities may not seem so terrible – after all, they are predictably available, easy to access, fast to forage, and can lead to increased condition and fertility among species that take advantage of them. For example, seabirds foraging among fishing boats for by-catch take advantage of the predictability of boat (and food) appearances and as a result have decreased foraging time and areas, higher individual fitness and reproductive success, and ultimately increased population growth. But the authors suggest that these benefits must be considered in a more complicated web of interactions. After all, human food subsidies tend to be much more predictable than natural sources of food and quickly have large effects spanning from individuals, communities, ecosystems, and evolutionary pressures.

Individuals often, though not always, experience positive effects from subsidies – increased biomass, fertility, and survival, accompanied by changes in dispersal and ranges. If food waste draws in high densities of individuals, it may be associated with greater disease occurrence, or draw in predators attracted to easy pickings. Populations also often respond positively to food subsidies, and become larger and more stable as food waste availability increases. But this boon for one species can cascade through the food web, and have large negative effects in communities and ecosystems. For example, yellow-legged gulls are found around dumps and fishing trawlers, taking advantage of the quantities of food available there, and as a result have increased greatly in population. The downside is that in turn these larger populations increase predation pressure on other vulnerable seabird species. Seabirds in particular can create complicated interactions between human food waste and far-flung ecosystems, connecting as they do both terrestrial and marine systems, moving nutrients, pollution, and calories between systems and through trophic levels.

Snow goose exclosure in northern Canada.
Only the small green rectangle has avoided goose grazing.

A famous example of the unexpected consequences of waste subsidies is the snow goose (Chen chen caerulescens). Snow geese have moved from feeding predominantly on marsh plants to landing en masse in farmers’ fields to feed on grain residues. This new and widespread source of food lead to a population boom, and the high numbers of geese stripped away the vegetation in the arctic habitats where they summer and breed. Agriculture food subsidies in southern habitats were felt far away in the arctic, as migratory snow geese tied these systems and food webs together. Though snow geese are unlikely to lose their new source of food, other animals may face plummeting populations or extinctions if food sources disappear. Until the 1970s, in Yellowstone, grizzly bears fed nearly exclusively at a local dump that then closed: the result was both increased mortality and rapid increases in foraging distances and behaviours.

Finally, and of most concern, food waste subsidies can alter the selective pressures a population faces. Species that become reliant on dumps or fields for food may experience changes in selective pressures, leading to selection for traits necessary to exploit these subsidies, and a loss of genotypic/phenotypic variation from the population. Changes in selective pressure change with the situation, of course. In the case of Yellowstone, the dump closure and loss of food source seemed to have large effects on traits important for sexual attractiveness in males, suggesting potential effects on reproductive success. In the best known (and my favourite) example of the selective effect of human food waste, dogs eventually were domesticated from wolf ancestors. Of course dumps can also relax selective pressures, if they allow individuals in poor condition (juveniles, the elderly) to successfully feed and reproduce.

Though food waste subsidies are clearly important and can have wide ranging effects, it is worth noting that the effect and importance of food subsidies is context-dependent. Studies seem to indicate that effects are greatest when food is low naturally or habitat quality is poor; in high quality systems, food waste may only be used by juveniles or individuals in poor condition. Unfortunately, as humans degrade natural habitats, subsidies are only likely to increase in importance as a food source for species. The extent and effects of human food waste are yet another legacy of the global alterations the human species has made. Unfortunately, like so many of the changes we have made, the issues are complex and transcend political and regional boundaries. Practices in one system or nation are tied to effects in another nation, and this complexity can make it difficult to monitor and measure the effects of subsidies as thoroughly as is necessary. This review from Oro et al. certainly makes a case for why our garbage needs to receive more attention.

One example of the ecosystem wide effects of subsidies: here, fisheries inputs.

Organic farming and natural enemy evenness

The basic reality of agricultural activity is that it reduces biological diversity, and these reductions in diversity potentially impact ecosystem services. But do some agricultural practices impact these services less than others? In a recent paper in Nature by David Crowder and colleagues, the question of how organic versus conventional farming affects predator and herbivore pathogen diversity and how this cascades to pest suppression. They show through a meta-analysis, that organic farms tend to support greater natural enemy evenness, and they hypothesize that greater evenness of enemies should better control pest populations, resulting in larger, more productive plants.

Picture from wikipedia

This result in itself is interesting, but they also carried out an elegant enclosure experiment where they manipulate the evenness of insect predators and pathogens and measure potato plant size. They found that even communities had the lowest herbivore densities and saw the greatest increases in plant biomass. Conversely, very uneven communities, typical of conventional farms, had the largest pest populations resulting in lower plant biomass accumulation.

While, multiple farming strategies are needed for adequate agricultural production, there are strong arguments for organic farms to be a important part of agricultural practice. These results show that organic farms have cascading effects on pest predators and pathogens and show that enemy evenness, as opposed to richness, has important ecosystem service consequences. To quote myself, evenness is a critical component of biodiversity, and much research has emphasized species richness, maybe at the detriment of studying evenness.

Crowder, D., Northfield, T., Strand, M., & Snyder, W. (2010). Organic agriculture promotes evenness and natural pest control Nature, 466 (7302), 109-112 DOI: 10.1038/nature09183