Phylogenetically-conserved candidate genes unify biodiversity-ecosystem function relationships and eco-evolutionary dynamics across biological scales

Abstract

The intra- and interspecific facets of biodiversity have traditionally been quantified and analysed separately, limiting our understanding of how evolution has shaped biodiversity, how biodiversity (as a whole) alters ecological dynamics, and hence eco-evolutionary feedbacks at the community scale. Here, we propose using candidate genes phylogenetically-conserved across species and sustaining functional traits as an inclusive biodiversity unit transcending the intra- and interspecific boundaries. This framework merges knowledge from functional genomics and functional ecology, and we first provide conceptual and technical guidelines for identifying phylogenetically-conserved candidate genes (PCCGs) within communities, and for measuring inclusive biodiversity from PCCGs. We then explain how biodiversity measured at PCCGs can be linked to ecosystem functions, which may unify recent observations that both intra- and interspecific biodiversity are important for ecosystem functions. We then highlight the eco-evolutionary processes shaping PCCGs diversity patterns, and argue that their respective role can be inferred from concepts derived from population genetics. Finally, we explain how PCCGs may shift the field of eco-evolutionary dynamics from a focal-species approach to a more realistic focal-community approach. This framework provides a novel perspective to investigate the global ecosystem consequences of diversity loss across biological scales, and how these ecological changes further alter biodiversity evolution.

Genetic diversity affects ecosystem functions across trophic levels as much as species diversity, but in an opposite direction

“…As such, it appears essential to maintain populations with high levels of genetic diversity in these ecosystems. Future studies should (i) extend these findings to other ecosystems and by quantifying natural genetic variation in more than a single species per trophic level, (ii) generate theoretical predictions regarding the mechanisms sustaining the antagonistic effects of genetic and species diversity on functions we revealed, and (iii) use a broader integrative approach for estimating biodiversity across facets (inclusive biodiversity) by using either a trait-based approach or a genetic-based approach as recently proposed by Blanchet et al (2023) and Loreau et al (2023). We focused on seven ecosystem functions associated with genetic and species diversity at three trophic levels (green for primary producer, orange for primary consumer and blue for secondary consumer).…”

“…Although natural assemblages encompass both intra-and interspecific diversity, most studies investigating BEFs are considering each biodiversity facet separately (but see, Fridley & Grime 2010;Prieto et al 2015). This makes it difficult to differentiate the relative role of genetic and species diversity in ecosystem functions, impeding general predictions regarding the consequences of biodiversity loss as a whole on ecosystem functions (Blanchet et al 2023). For instance, we are currently unaware whether genetic diversity may functionally compensate for a species loss in an (species-poor) ecosystem, whether the loss of genetic diversity within a few species in an assemblage is as detrimental for ecosystem functions as a species loss, or whether the combined loss of genetic and species diversity may have non-additive consequences for ecosystem dynamics.…”

Genomic and species diversity patterns across multiple trophic levels in riverscapes

“…Finally, it is possible that spatial co-variation between genomic and species diversity might be revealed more precisely by shifting from a 'single target species' approach (genomic diversity is inferred from a single species) to a 'multiple target species' approach (genomic diversity is inferred from a several species). This could be done for instance by 1) estimating spatial covariation between species diversity and the average genomic diversity of several species within the community, and/or 2) estimating genomic diversity jointly from all species within the focal community by sequencing genes that are phylogenetically conserved across species (Blanchet et al 2022). To answer these questions (and others), we encourage scientists to integrate multiple trophic levels and multiple facets of biodiversity to future empirical and theoretical studies to better understand the spatial distribution of biodiversity, the underlying processes that shape biodiversity on Earth, and their consequences on ecosystem functioning.…”

“…Yet, these two facets of biodiversity are actually forming a single entity, as variation observed within species eventually leads to speciation over the long-term. Developing approaches to jointly understand the processes shaping these biodiversity facets may significantly improve our perception of biodiversity (Vellend and Geber 2005, Coates et al 2018, Blanchet et al 2022.…”

Editorial 2024

“…Blanchet et al. (2023) put forward a framework—based on analyses of phylogenetically conserved candidate genes and associated functional traits—for investigating eco‐evolutionary processes across biological scales.…”