Definition of phylogenetically-conserved candidate genes
PCCGs are genes identified by functional biologists as having major
effects on traits, and whose sequence and function are (at least partly)
conserved across a broad range of species. This concerns genes coding
for ecologically important traits, for instance traits associated
(directly or indirectly) to resource acquisition or to interactions with
other organisms
(Skovmand et
al. 2018). Many PCCGs have been identified by functional biologists,
but this knowledge has poorly percolated into our scientific community,
but for rare exceptions such as behavioural ecology
(e.g., Fitzpatricket al. 2005; Ducrest et al. 2008). We believe that we
should build on this knowledge, and that PCCGs may be fundamental to
unify facets of biodiversity.
Seminal works from the 90’s have identified candidate genes sustaining
traits that matter for fitness
(Andersen &
Lübberstedt 2003; Meinke et al. 2008; Chu et al. 2011;
Schwander et al. 2014; Hassani-Pak & Rawlings 2017; Anreiter &
Sokolowski 2019). In animals, some of these genes code for functional
traits, such as foraging behaviour, metabolism or stoichiometry, that
are strongly related to the acquisition of resources and/or its
conversion into biomass
(Brown et al.2004; Violle et al. 2007; Wolf & Weissing 2012). For instance,
the Sokolowski’s team identified a gene (the for gene) strongly
controlling the foraging behaviour of Drosophila melanogaster(de Belle et
al. 1989; Sokolowski 2001; Anreiter & Sokolowski 2019). This gene
codes for a cGMP-dependent protein kinase (a signalling molecule) and
encodes two main behavioural strategies: the rover strategy describingDrosophila larvae travelling long distance to feed, and the
sitter strategy describing Drosophila larvae feeding in more
restricted areas. This gene also impacts the food intake of individuals
(rover larvae have lower food intake) and the food preference (rover
larvae absorb higher glucose quantities) (Anreiter & Sokolowski 2019).
We can reasonably expect that variation in the expression of this gene
will have consequences on trophic chains, and ecosystem functioning. For
plants, MADS-box genes described in Antirrhinum majus(Schwarz-Sommeret al. 1990) are a family of genes encoding transcription
factors involved in flowering time, plant and floral architecture, and
fruit, seed and root development
(Schilling et
al. 2018). MADS-box genes are key targets to improve crops’ yields,
and are altering the short term adaptation of plants to environmental
changes (Cho et
al. 2017; Theißen et al. 2018). For instance, the Flowering
Loci C and T regulate flowering time in many plant species, an important
trait for individual fitness, and for the function of pollination by
insects (Schmidtet al. 2016).
This type of candidate genes is similar to (and is therefore
reinforcing) the idea of “Ecology Important Genes” (EIG) (Skovmandet al . 2018), defined as genes contributing strongly to
phenotypes having a large effect on communities and ecosystems.
Nonetheless, we stress that the purpose of our approach –contrary to
Skovmand et al . (2018)– is not to search for rare EIGs with
disproportionately large effects (what they called Keystone Genes, KGs),
but rather to consider the impacts of a large number of these candidate
genes (a hundred or more) with small to large individual contributions
to traits and to ecological dynamics. Our approach acknowledges the idea
that phenotypes likely arise from the collective effect of many genes
with small effect sizes
(Falconer 1981).
Focusing on a large number of candidate genes should also offer the
opportunity to identify complementarity and redundancy (in
term of trait functions, see BOX 1) among genes or locus within a
community, which are two important concepts for predicting the impacts
of biodiversity on ecological processes
(Loreau 1998).
An important aspect of our framework is that we focus on candidate genes
that are phylogenetically conserved , meaning that they can be
sequenced across a large range of species within communities. The fact
that genes are ecologically important is not sufficient to warrant their
integration across the intra-/interspecific biodiversity facets; they
must also be phylogenetically conserved. Noteworthily, most candidate
genes identified in model species are actually conserved (at least
partly) across species. For instance, the for gene is extremely
conserved, and its sequence can be retrieved from a large number of
Invertebrate species
(Sokolowski 2001;
Anreiter & Sokolowski 2019). An ortholog -i.e., a gene whose the
sequence has diverged over the course of evolution from a shared genetic
ancestor- gene (PRKG1 ) identified in Vertebrates was found
associated with foraging-like behaviour in humans, amphibians and small
mammals (Anreiter &
Sokolowski 2019; Struk et al. 2019). Similarly, the MADS-box
gene complex has been identified in many taxonomic groups including
mosses, gymnosperms and angiosperms
(Gramzow & Theißen
2013; Schilling et al. 2018). Conservatism of candidate traits
should actually be the norm rather than the exception given their
importance for essential biological functions
(Marden et al.2013; Barson et al. 2015; McGirr & Martin 2016; James et
al. 2017).
Using PCCGs as target for measuring biodiversity inclusively is
particularly attractive because the dynamics of PCCGs is shaped by
demographic and (micro- and macro-) evolutionary processes, and because
PCCGs likely code for important ecological traits and functions linked
to ecological processes. PCCGs are therefore at the intersection of
ecological and evolutionary dynamics, which makes them an ideal basis to
identify new mechanisms linking the environment, biodiversity and the
functioning of ecosystems. Hereafter, we provide insights into the
concepts and tools currently available to inform PCCG diversity across
species, and we provide a technical framework that forms the basis of
future research (Figure 2).