Abstract
Despite their close links, ecology and evolution have remained separate
disciplines to this day. Breaking down the wall between the two
disciplines is essential for at least two reasons. First, this wall is
an obstacle to the study of most microorganisms, which constitute a
large part of the Earth’s biodiversity. Asexual reproduction, gene
transfer and the lack of a clear definition of the species taxonomic
level blur the distinction between ecological changes in species
abundances and evolutionary changes in genotype frequencies in microbes.
Second, a key question that biodiversity science will have to address in
the coming decades is how ecological systems will cope with rapid
environmental change. Generalising the concept of adaptation across
multiple timescales and levels of organisation would provide an
integrative framework for studying the combined ecological and
evolutionary responses to environmental change, and thus help us to
address one the major scientific challenges of our time.
Although Darwin, the father of modern evolutionary biology, had a strong
interest in ecological issues, ecology and evolution developed
historically as separate scientific disciplines, each with its own set
of concepts, methods and study objects (Futuyma 1986). While ecology is
broadly concerned with the interactions between living organisms and
their biotic and abiotic environment, evolutionary biology focuses on
changes in the intrinsic characteristics, or traits, of these organisms
through time under changing environments. As a result of this focus,
evolutionary biology built a coherent body of theory that gave rise to
the so-called “modern synthesis”. This synthesis integrated knowledge
from genetics, palaeontology, systematics and morphology, but ecology
played a relatively small role, although the influence of ecological
processes on evolution was recognised (Huneman 2019). By contrast,
ecology developed a wide range of perspectives, from the dynamics of a
single population to the functioning of the entire biosphere, but it is
arguably still searching for a general synthesis (Loreau 2010). Despite
the close links between ecological and evolutionary processes, ecology
and evolution have remained separate disciplines to this day.
The traditional separation between ecology and evolution assumes that
the timescales of ecological and evolutionary processes differ,
evolution being slower than ecological dynamics. This assumption has
been challenged by recent studies showing that evolution can be rapid,
leading to an interplay of ecological and evolutionary dynamics known as
“eco-evolutionary dynamics” (Fussmann et al. 2007; Schoener
2011; Hendry 2020). The field of eco-evolutionary dynamics has greatly
contributed to strengthening the links between ecology and evolution by
revealing how ecology affects evolution and, conversely, how evolution
affects ecology, leading to potential eco-evolutionary feedbacks. We now
know that emergent properties of communities and ecosystems, such as
material cycling, functional complementarity between species and
community stability, have the potential to affect evolutionary
processes, just as evolution can affect ecosystem functioning (Loreau
2010; Borrelli et al. 2015; Calcagno et al. 2017; Aubreeet al. 2020). Despite growing awareness of the interactions
between ecological and evolutionary processes, however, there remains a
wide gap between ecology and evolution, both in terms of concepts and
study objects. Even in eco-evolutionary dynamics, ecology is often
reduced to changes in the abundance of species or phenotypes, while
ecosystem processes and abiotic factors are more background than genuine
actors.
Here we argue that breaking down the wall between the two disciplines is
essential for at least two major reasons: (1) this wall is an obstacle
to the study of most microorganisms, which constitute a large part of
the Earth’s biodiversity; (2) understanding and predicting the response
of biodiversity and ecosystems to environmental change requires a more
integrative view of ecological and evolutionary processes. In the
current context of accelerating environmental change, we discuss why
microorganisms are ideal systems for revisiting the deep links between
ecology and evolution. We also discuss how some concepts such as
adaptation could serve as tools for a fruitful dialogue in the
convergence between the two disciplines.
The separation between ecology and evolution implicitly assumes not only
that the timescales considered differ, but also, more fundamentally,
that within-species evolutionary processes can be neatly separated from
between-species ecological processes. While these distinctions in
timescales and levels of biological organisation may generally make
sense for large, complex, sexually reproducing multicellular eukaryotes,
they are far less relevant for bacteria, archaea and other microbes,
where asexual reproduction and gene transfer are widespread and thus the
distinction between ecological and evolutionary processes is blurred.
Although asexual reproduction and gene transfer do not preclude a
taxonomic classification of microbes as microbial traits are
phylogenetically conserved in a hierarchical fashion (Martiny et
al. 2015), the species level in this hierarchy is ill-defined and
largely arbitrary. Therefore, there is no fundamental difference between
changes in the abundance of different microbial “species” through time
— the traditional focus of community ecology — and changes in the
relative frequency of different microbial “genotypes” — the
traditional focus of evolution. Indeed, some classic examples of
eco-evolutionary dynamics, such as Yoshida et al.’s (2003) predator−prey
cycles driven by the “rapid evolution” of clonal algae, could be
easily reinterpreted as simple ecological dynamics in which the
abundance of different algal “species” changes. A similar issue arises
in clonal multicellular organisms (e.g. parthenogenetic freshwater
snails: Facon et al. 2008). Changes in species abundances and
changes in phenotype frequencies generate the same type of effect, i.e.
changes in mean trait values. Whether these changes in mean trait values
take place at the population or community level is largely irrelevant in
the case of microbes, as the two hierarchical levels cannot be
distinguished unambiguously. Note that this also challenges the
distinction between intra- and interspecific competition, which is
widely regarded as the key factor explaining the maintenance of
biodiversity (Chesson 2000). Widespread gene transfer is another aspect
that makes the distinction between ecology and evolution much more
blurred in microbes than in macroorganisms. Given the enormous
abundance, phylogenetic diversity and functional importance of microbes,
they should be considered more than a curiosity in evolutionary biology
or an exceptional model for experimental evolution (Lenski 2017).
Microbes invite us to rethink the boundaries and interactions between
ecology and evolution, and we feel this invitation should be seen as a
great opportunity rather than a problem.
Perhaps nowhere is cross-fertilisation between the two disciplines more
important than in fostering a better understanding of current and future
changes in biodiversity and ecosystems at a time when the impact of
human activities on the biosphere is rapidly increasing. Climate change
seems to have already acted as a catalyst for eco-evolutionary studies
(Hendry 2020). The ongoing anthropogenic environmental changes are so
widespread, rapid and profound that the historically inherited
distinction between ecology and evolution might soon become at best
irrelevant, at worst an obstacle to our understanding of the
consequences of these changes. One of the main questions that
biodiversity science will have to address in the coming decades is how
ecological systems will cope with rapid environmental change: Which
communities or ecosystems will adapt and persist, and which will
collapse? What will be the characteristics of the new communities or
ecosystems that emerge? Answering these questions in detail will require
careful dissection of the various evolutionary and ecological mechanisms
at work, but in many circumstances, this will not be possible due to
limited time and resources. Again, microbes are a case in point.
Although careful experimental studies can unravel the respective roles
of demographic and evolutionary responses to environmental change in at
least some bacteria (Chase et al. 2021), the microscopic spatial
and temporal scales at which changes in microbial communities occur, the
fact that many bacteria cannot be cultured, and the lack of a clear
definition of the species concept in microbes make it unrealistic to
expect to be able to clearly separate ecological and evolutionary
responses to environmental change in most microbiomes.
In the face of these conceptual and technical obstacles, many concepts
used in either ecology or evolution could be profitably applied in the
other discipline, provided that their definition is generalised in a
relevant and consistent way. In particular, adaptation is a concept that
is mainly used in evolution, but is very relevant to ecology. In
evolution, ‘adaptation’ sensu stricto is generally considered as
a process leading to higher fitness as a result of natural selection
(Williams 1966; Gardner 2017), while ‘adaptedness’ denotes the state of
being adapted, but the distinction is not always so clear (Lewens 2016).
Even in the writings of such a strong proponent of individual-level
selection as Williams (1966), ‘organic adaptations’ could be
distinguished from ‘biotic adaptations’, which help perpetuate a group
or population. It would be particularly useful to extend and generalise
the concept of adaptation to wider ecological contexts. Soil microbial
ecologists have begun to use this concept at the community level to
describe an increase in overall microbial activity as temperature
changes, an approach that integrates across the mechanisms and
timescales involved (Bradford 2013; Nottingham et al. 2021). This
extension of the adaptation concept is fully consistent with that
formally proposed by hierarchical adaptability theory (Conrad 1983;
Lekevičius & Loreau 2012). Hierarchical adaptability theory regards
adaptation as a multilevel hierarchical process that involves a range of
adaptive responses to environmental changes, from molecules to
ecosystems. These responses include differential gene activity
(molecular-level mechanism), phenotypic plasticity (individual-level
mechanism), differential reproduction of genotypes (population-level
mechanism), and changes in species abundances (community- or
ecosystem-level mechanism). In this theory, the adaptation concept is
generalised to refer to any process that results in improved performance
in response to environmental change. The concept could be further
extended to denote the evolutionary, ecological, and social changes that
reduce the vulnerability of social and ecological systems to
environmental change (Moore & Schindler 2022).
These extensions, of course, raise the question of how to measure
performance below or above the hierarchical level of the individual
organism. In evolutionary theory, performance is encapsulated in the
concept of fitness. Defining the performance of a community or ecosystem
seems challenging because communities and ecosystems are not
superorganisms (Loreau 2010). This difficulty, however, may not be as
great as it first appears. First, the well-accepted fitness concept is
also notoriously difficult to define and measure a priori in
evolutionary theory. In particular, it is critical to define fitness as
a potential, not a realised property, if it is to have any explanatory
power (Brandon 1990; Orr 2009), a criterion that should apply to any
performance indicator at any biological level. Second, many ecosystem
processes, such as resource uptake, primary production, secondary
production and material cycling efficiency, are closely linked (Loreau
2010), so that different measures of ecosystem performance may often
provide broadly consistent results when assessing the response of an
ecosystem to abrupt environmental changes. Third, current environmental
changes are likely to shed new empirical light on this issue in the near
future by pushing ecosystems beyond critical thresholds, leading to
major, readily observable changes in ecosystem structure and
functioning. Interestingly, recent ecological theory predicts that
simple competitive communities with high variance in species interaction
strength behave somewhat like superorganisms along environmental
gradients, with abrupt species turnover and sharp boundaries between
communities, despite the absence of strong functional integration
(Liautaud et al. 2019). Furthermore, these communities can
exhibit directional dynamics in time, i.e., they are characterised by a
maturity function that systematically increases over time, as well as
community-level selection in space, i.e. they expand across space by
replacing other communities with copies of themselves (Bunin 2021).
One might object that there is currently limited evidence for abrupt
ecological responses to environmental changes (Hillebrand et al.2020). This empirical argument, however, may soon become obsolete. In
particular, changes in plant and animal community composition are
lagging behind current climate warming, generating a significant
climatic debt (Bertrand et al. 2011). As climate warming is
expected to accelerate during this century, this climatic debt is likely
to increase, eventually leading to the collapse of existing communities
before being possibly replaced by new ones. Other drivers of changes in
biodiversity and ecosystems, such as habitat loss and fragmentation,
invasive species, overharvesting and pollution, are likely to combine
with climate change to form a ‘deadly anthropogenic cocktail’ (Travis
2003). Thus, it seems clear that most abrupt ecological changes are yet
to come.
Successful integration of ecology and evolution requires a careful
assessment of the scales and hierarchical levels at which the various
ecological and evolutionary processes operate, and how they interact or
combine. But the generalisation of basic concepts such as adaptation
across scales and hierarchical levels would be a particularly useful
effort — they would serve as ‘boundary objects’ (Star & Griesemer
1989) in the conceptual unification of ecology and evolution. Other
concepts, such as stability, resilience and resistance, which are
commonly used in ecology, could also be applied to evolutionary systems
(Nosil et al. 2021), provided that their definitions are clear
and consistent. The effort is well worth it, as breaking down the wall
between ecology and evolution would bring enormous benefits. In
particular, it would help us to address one the major scientific
challenges of our time — to understand and predict changes in
biodiversity in the face of rapid environmental change, especially in
microbiomes, which play a key role in all biological and ecological
processes, from the health of individual organisms to the functioning of
the biosphere as a whole.