Decomposing diversity effects within species

The relationship between biodiversity and ecosystem functioning is so frequently discussed in the ecological literature that it has its own ubiquitous acronym (BEF). The literature has moved from early discussions and disagreements about mechanism, experimental design, and species richness to ask how different components of biodiversity might contribute differentially to functioning. The search is for mechanisms which hopefully will lend predictability to biodiversity-function relationships. One approach is to independently manipulate different facets of biodiversity – whether species, phylogenetic, trait-based, or genetic diversity – to help disentangle the relative contribution of each.

A new paper extends this question by considering how within-species diversity – including genotypic richness, genetic differences, and trait differences – contribute to functioning. Abbott et al. (2017, Ecology) use a field-based eelgrass system to explore how independent manipulations of genotypic richness and genetic relatedness affected biomass production and invertebrate community richness. They collected 41 unique genotypes of eelgrass (Zostera marina), and used 11 species-relevant loci to determine the relatedness of each genotype pair. The authors also measured 17 traits relevant to performance including "growth rate, nutrient uptake, photosynthetic efficiency, phenolic content, susceptibility to herbivores, and detrital production ".

Eelgrass meadow.
From
http://www.centralcoastbiodiversity.org/
eelgrass-bull-zostera-marina.html

Each of these of these measures are inter-related, but not necessarily in clear, predictable fashions. Genotypes likely differ functionally, but some traits and some genotypes will vary more than others. Genetic distances or relatedness between species similarly may be proxies for trait differences, but this depends on the underlying evolutionary processes. The relationship between any of these measures and functions such as biomass production are no doubt varied and dependent on the mechanism.

The authors established plots with two levels of genotypic richness, either 2 genotypes or 6 genotypes, where genotypes varied among the 41 available. Fully crossed with the genotypic richness treatment was a genetic relatedness treatment: genotypes were either more closely related than a random selection, less closely related, or as closely related as random. At the end of the experiment, above and belowground biomass were collected, and epifaunal invertebrates were collected, and modelled as a component of the biodiversity components.

Because of early die-offs in many plots, planted genotype richness differed from final richness greatly (very few plots had 6 genotypes remaining, for example). For that reason, final diversity measures were used in the models. The relationship between aboveground biomass or belowground biomass and biodiversity were similar: both genotypic richness and genotypic evenness were positively related to total final biomass, but genetic relatedness was negatively correlated. That is, plots with more related genotypes were less productive. Other variables such as trait diversity was not as important, and in fact they did not find any relationship between trait differences and degree of genetic relatedness between genotypes. Since relatedness seemed unrelated to functional similarities, between genotypes, the authors suggested that possibly that reduced biomass among related genotypes is due to self-recognition mechanisms. Most interestingly, the best predictors of invertebrate grazer diversity were opposite -  – the best predictor was trait diversity, not genotypic richness or genetic relatedness.

Even in this case, where Abbott et al. were able to separate different diversity components experimentally, it's clear that simplistic predictions as to how they contribute to functioning are insufficient. The contributions of genotypic versus trait diversity were not strongly related. Further, trait diversity performed best on the function for which genotypic diversity performed worst. Understanding what this means is difficult - are the traits relevant for understanding intraspecific interactions (resource usage, etc) so incredibly different from those relevant for interspecific interactions with herbivores? Are the 17 traits too few to capture all differences, or too many irrelevant traits? Do we expect different biodiversity facets have unique independent effects on ecosystem functions, or does the need to consider multiple facets simply mean we have an imperfect understanding of how different facets are related? 

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.

Plant genotypic diversity supports pollinator diversity

Research over the past 20 years has shown that plant communities with greater diversity maintain higher productivity, greater stability and support more diverse arthropod assemblages. More recently, several experiments have shown that interspecific diversity (namely genotypic differences) also affects community functioning. Pollination is often considered an essential function, and does plant genotypic diversity affect pollinator diversity and frequency?

In a recent paper in PLoS ONE, Genung and colleagues test whether plant genotypic diversity affects pollinator visits. They use an experimental system set-up by Greg Crutsinger that combines multiple genotypes of the goldenrod, Solidago altissima, and record pollinator visits over two years. Experimental plots contained 1, 3, 6, or 12 genotypes of S. altissima. After accounting for differences in abundance, Genung et al. show that as genotypic diversity increases, both pollinator richness and number of visits to the plot significantly increase. This increase is greater than expectations of randomly simulated assemblages combining proportional pollinator visits from monocultures.

The previous research at the species-level has made a persuasive rationale to protect species diversity in order to maintain ecosystem functioning. Now, research like this is making a case that there are consequences for not explicitly considering genetic diversity in conservation planning and habitat restoration.

Genung, M., Lessard, J., Brown, C., Bunn, W., Cregger, M., Reynolds, W., Felker-Quinn, E., Stevenson, M., Hartley, A., Crutsinger, G., Schweitzer, J., & Bailey, J. (2010). Non-Additive Effects of Genotypic Diversity Increase Floral Abundance and Abundance of Floral Visitors PLoS ONE, 5 (1) DOI: 10.1371/journal.pone.0008711