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).