We present evidence that the heritable genetic variation within individual species, especially dominant and keystone species, has community and ecosystem consequences. These consequences represent extended phenotypes, i.e., the effects of genes at levels higher than the population. Using diverse examples from microbes to vertebrates, we demonstrate that the extended phenotype can be traced from the individuals possessing the trait, to the community, and to ecosystem processes such as leaf litter decomposition and N mineralization. In our development of a community genetics perspective, we focus on intraspecific genetic variation because the extended phenotypes of these genes can be passed from one generation to the next, which provides a mechanism for heritability. In support of this view, common‐garden experiments using synthetic crosses of a dominant tree show that their progeny tend to support arthropod communities that resemble those of their parents. We also argue that the combined interactions of extended phenotypes contribute to the among‐community variance in the traits of individuals within communities. The genetic factors underlying this among‐community variance in trait expression, particularly those involving genetic interactions among species, constitute community heritability. These findings have diverse implications. (1) They provide a genetic framework for understanding community structure and ecosystem processes. The effects of extended phenotypes at these higher levels need not be diffuse; they may be direct or may act in relatively few steps, which enhances our ability to detect and predict their effects. (2) From a conservation perspective, we introduce the concept of the minimum viable interacting population (MVIP), which represents the size of a population needed to maintain genetic diversity at levels required by other interacting species in the community. (3) Genotype × environment interactions in dominant and keystone species can shift extended phenotypes to have unexpected consequences at community and ecosystem levels, an issue that is especially important as it relates to global change. (4) Documenting community heritability justifies a community genetics perspective and is an essential first step in demonstrating community evolution. (5) Community genetics requires and promotes an integrative approach, from genes to ecosystems, that is necessary for the marriage of ecology and genetics. Few studies span from genes to ecosystems, but such integration is probably essential for understanding the natural world. Corresponding Editor: A. A. Agrawal
The genus Populus consists of dioecious woody species with largely unknown genetic mechanisms for gender determination. We have discovered genetic and genomic features in the peritelomeric region of chromosome XIX that suggest this region of the Populus genome is in the process of developing characteristics of a sex chromosome. We have identified a gender-associated locus that consistently maps to this region. Furthermore, comparison of genetic maps across multiple Populus families reveals consistently distorted segregation within this region. We have intensively characterized this region using an F 1 interspecific cross involving the female genotype that was used for genome sequencing. This region shows suppressed recombination and high divergence between the alternate haplotypes, as revealed by dense map-based genome assembly using microsatellite markers. The suppressed recombination, distorted segregation, and haplotype divergence were observed only for the maternal parent in this cross. Furthermore, the progeny of this cross showed a strongly male-biased sex ratio, in agreement with Haldane's rule that postulates that the heterogametic sex is more likely to be absent, rare, or sterile in interspecific crosses. Together, these results support the role of chromosome XIX in sex determination and suggest that sex determination in Populus occurs through a ZW system in which the female is the heterogametic gender.
While population genetic diversity has broad application in species conservation, no studies have examined the community-level consequences of this diversity. We show that population genetic diversity (generated by interspecific hybridization) in a dominant riparian tree affects an arthropod community composed of 207 species. In an experimental garden, plant cross type structured the arthropod community of individual trees, and among stands in the wild, plant genetic diversity accounted for nearly 60% of the variation in arthropod diversity. While previous experimental garden studies have demonstrated the effects of plant genotype on arthropod communities, our study extends these findings from individual trees in an experimental garden to natural stands of cottonwoods where plant population genetic diversity was a significant factor structuring arthropod diversity. These findings argue that the preservation of genetic diversity in a dominant species is far more important than previously realized, and may be particularly important in hybridizing systems.
Summary Restoration is normally conducted with the goal of creating plant populations that establish, survive, successfully reproduce, contribute to ecosystem function and persist in the long term. Restoration often relies on revegetation that, on large scales, requires agronomic increase of native plant materials. During this propagation process, restoration populations are subject to genetic sampling as well as natural and artificial selection that could result in adaptation contrasting sharply with that of native populations. Here we draw on insights from the evolutionary and agricultural literature to illustrate how changes in the amount and type of genetic variation in ex situ repositories (source collections and production farms) could affect plant performance in restoration. The consequences of intentional and/or inadvertent evolutionary modification of restoration materials are discussed with respect to population viability and ecosystem function. Synthesis and applications. We conclude that sampling effects and intentional and unintentional selection during collection, propagation and restoration planting have the potential to diminish restored populations. We describe testing for evolutionary change in plant materials using neutral molecular markers and/or field observations. Six practices, multiple collections through time, multiple collections through space, large effective population size, provenance tracking, promoting gene flow and reducing selection comprise ‘evolutionarily enlightened management’ that decreases the potential for unintentional evolution and maladaptation.
An important step in the integration of ecology and genomics is the progression from molecular studies of relatively simple model systems to complex field systems. The recent availability of sequenced genomes from key plants is leading to a new understanding of the molecular drivers of community composition and ecosystem processes. As genome sequences accumulate for species that form intimate associations in nature, a detailed view may emerge as to how these associations cause changes among species at the nucleotide level. This advance could dramatically alter views about the structure and evolution of communities and ecosystems.
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