Introduction
Global change is modifying worldwide patterns of biodiversity (Parmesan & Yohe 2003; Newbold et al. 2015). The rate of species loss is so rapid that it is actually called the 6th mass extinction (Barnosky et al. 2011). Nonetheless, biodiversity changes do not only concern species loss, but also the loss of the diversity characterising (almost) every species, i.e., intraspecific diversity. Genes and life-history strategies are being lost within species, because humans are altering fundamental processes impairing intraspecific diversity (Spielman et al. 2004; Hendry et al. 2008; Leigh et al. 2019). The loss of intraspecific diversity always precedes (and potentially speeds up) species loss (Spielman et al. 2004); it is hence essential to consider biodiversity loss as aninclusive process occurring across genes and species (Bellard et al.2012).
Nonetheless, in most studies, the intra- and interspecific facets of biodiversity are treated as separate entities (but see e.g., Start & Gilbert 2019), while they actually form an evolutionary continuum. This limits our ability to provide an integrative perspective of eco-evolutionary relationships between biodiversity, the environment and ecosystem functioning (Matthews et al. 2011). This gap between biodiversity facets has historical causes since intraspecific diversity has mainly been studied through a population geneticist lens, whereas interspecific diversity has mainly been studied by community ecologists. This gap has progressively been conceptually concealed with the recognition of tight links between ecological and evolutionary dynamics (Hubbell 2001; Whithamet al. 2003; Vellend 2005; Whitham et al. 2008; Matthewset al. 2014). It also has an intrinsic cause since intra- and interspecific diversity are quantified using different units. Interspecific diversity is generally measured as the number of species, whereas intraspecific diversity can be estimated through metrics of genetic (allelic richness, heterozygosity…) and phenotypic diversity (trait variance, number of ecotypes…), which impedes the inclusive measurement of biodiversity within communities. Some studies have proposed common statistical frameworks to jointly measure intra- and interspecific diversity within communities (e.g., Pavoine & Izsák 2014a; Gaggiotti et al. 2018; Carmona et al. 2019), demonstrating the scientific ambition to transcend the intra-/interspecific boundary. However, these attempts are rare, and they have not been developed with the initial objective of linking theseinclusive metrics of biodiversity to both ecological and evolutionary dynamics.
Developing a biodiversity unit transcending the intra-/interspecific boundary and allowing for an inclusive measurement of biodiversity has many implications such as, changing our perspective on the links between biodiversity and ecosystem functioning. Biodiversity sustains key ecosystem functions such as primary productivity or recycling of dead organic matter (Chapinet al. 2000; Loreau et al. 2001; Hooper et al.2005). These links between biodiversity and ecosystem functioning (“BEF”) rest on the idea that higher levels of biodiversity promote higher trait complementarity among individuals and/or increase the likelihood to sustain highly competitive traits with dominant effects (see BOX 1), both processes maximising resource acquisition and its conversion into biomass or energy (Hooper et al.2005). BEF relationships have been historically described at theinterspecific level, and seminal experiments have demonstrated that higher plant species richness in communities increases and stabilises yields (Tilman et al.1996, 2006; Chapin et al. 1997). More recently, similar observations have been reported at the intraspecific level; plant or animal populations composed of a large number of genotypes sustain higher yields and community diversity than populations with a poor genotypic diversity (e.g., Hughes & Stachowicz 2004; Reusch et al. 2005; Crutsinger et al.2006; Raffard et al. 2021). Altogether, this suggests that both losing alleles within populations and species within communities can alter the functioning of ecosystems. Yet, the dichotomy between intra- and interspecific diversity impedes a global assessment of biodiversity loss on ecosystem dynamics (but see, e.g., Prietoet al. 2015).
The use of an inclusive biodiversity unit should also ease our understanding of how ecology affects the evolution of organisms (andvice versa ) composing communities. The ecological effects generated by trait variation described above can feedback to evolutionary processes when these ecological effects affect the selective regime and/or demographic parameters, which has been termed “eco-evolutionary dynamics” (Thompson 1998; Schoener 2011; Hendry 2017). Revealing eco-evolutionary dynamics requires tracking the allele frequencies -within communities- of genes sustaining traits that are impacting -and reciprocally impacted by- ecological processes (Lowe et al.2017; Skovmand et al. 2018). Although allele frequencies can “easily” be tracked in a single focal species from a community (Lowe et al.2017; Rudman et al. 2018), this becomes far more complicated when it comes to allele frequencies from genes of all species from a community, which is however what reality is (De Meester et al. 2019; Hendry 2019). Our dichotomic perception of intra- and interspecific diversity limits our capacity to built-up and understand eco-evolutionary dynamics beyond a (few) focal species within communities, which hence minimises the relevance of the eco-evolutionary framework for predicting the consequences of global change on biological dynamics.
Here, we propose that candidate genes that are phylogenetically conserved across taxa and that sustain key functional traits may serve as an inclusive biodiversity unit unifying the intra- and interspecific diversity components (Figure 1). We argue that this genetic metric of inclusive biodiversity may explain ecological processes, and may allow tracing eco-evolutionary dynamics directly from genes that are found in most species of a local community and that are important for ecological processes. Phylogenetically-conserved candidate genes are here defined as genetic sequences coding for important ecological traits (e.g., resource acquisition and transformation) and that are conserved across a broad range of organisms. Thanks to the development of high-throughput sequencing approaches, the diversity of hundreds of these genes can be revealed at the intra- and interspecific levels simultaneously, providing the raw material for a genome -and community- wide measure of biodiversity. As the dynamics of candidate genes is shaped by evolutionary processes, and as they code for important traits, they constitute an ideal basis to set new perspectives on the links between the environment, biodiversity and the functioning of natural ecosystems, as well as on biodiversity conservation.
In this Perspective, we first develop the rationales motivating our idea that phylogenetically-conserved candidate genes (PCCGs) are ideal targets to unify biodiversity metrics across scales, we present examples from functional biology having linked these genes to ecologically important traits. We further provide technical guidelines regarding the methods available to sequence these genes and to estimate an inclusive metric of biodiversity from these genes. We finally expand on the main implications of measuring the diversity of PCCGs in natural (or experimental) communities, in particular for predicting the functioning and stability of ecosystems, for revealing the demographic and evolutionary processes shaping patterns of biodiversity, and for dissecting and tracing the feedbacks between ecological and evolutionary dynamics at the focal-community level (Figure 1).