Eco-evolution from deep time to contemporary dynamics the role of timescales and rate modulators

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Eco-evolution from deep time to

contemporary dynamics: the role of

timescales and rate modulators

Emanuel A. Fronhofer1, Dov Corenblit2,3, Jhelam N. Deshpande1, Lynn Govaert4, Philippe Huneman5,

Fr´ed´erique Viard1, Philippe Jarne6and Sara Puijalon7

1. ISEM, Universit´e de Montpellier, CNRS, IRD, EPHE, Montpellier, France

2. Universit´e Clermont Auvergne, CNRS, GEOLAB – F-63000 Clermont-Ferrand, France

3. CNRS, Laboratoire ´ecologie fonctionnelle et environnement, Universit´e Paul Sabatier, CNRS, INPT,

UPS, F-31062 Toulouse, France

4. Leibniz Institute of Freshwater Ecology and Inland Fisheries, M¨uggelseedamm 310, 12587 Berlin,

Germany

5. Institut d’Histoire et de Philosophie des Sciences et des Techniques (CNRS/ Universit´e Paris I

Sorbonne)

6. CEFE, UMR 5175, CNRS - Universit´e de Montpellier - Universit´e Paul-Val´ery Montpellier - IRD

- EPHE, 1919 route de Mende, 34293 Montpellier Cedex 5, France

7. Univ Lyon, Universit´e Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, F-69622,

Villeurbanne, France

Running title: Eco-evolution, timescales and modulators

Keywords: eco-evolutionary feedback, geomorphology, contemporary evolution, key innovation, multi-

layer networks, ecological opportunity, speciation, global change, emergence, ecosystem genetics

Author contributions: Conceptualization: E.A.F., P.J., S.P., D.C., F.V.; Visualization: E.A.F.,

P.J., L.G., D.C.; Writing – original draft: E.A.F., P.J., J.N.D., P.H., D.C., S.P.; Writing – review &

editing: all authors.

Correspondence Details

Emanuel A. Fronhofer

Institut des Sciences de l’Evolution de Montpellier, UMR5554

Universit´e de Montpellier, CC065, Place E. Bataillon, 34095 Montpellier Cedex 5, France

phone: +33 (0) 4 67 14 31 82

email: emanuel.fronhofer@umontpellier.fr

arXiv:2210.12041v1 [q-bio.PE] 21 Oct 2022

Abstract

Eco-evolutionary dynamics, or eco-evolution for short, are thought to involve rapid demography (ecology)

and equally rapid phenotypic changes (evolution) leading to novel, emergent system behaviours. This

focus on contemporary dynamics is likely due to accumulating evidence for rapid evolution, from classical

laboratory microcosms and natural populations, including the iconic Trinidadian guppies. We argue

that this view is too narrow, preventing the successful integration of ecology and evolution. While

maintaining that eco-evolution involves emergence, we highlight that this may also be true for slow ecology

and evolution which unfold over thousands or millions of years, such as the feedbacks between riverine

geomorphology and plant evolution. We thereby integrate geomorphology and biome-level feedbacks into

eco-evolution, signiﬁcantly extending its scope. Most importantly, we emphasize that eco-evolutionary

systems need not be frozen in state-space: We identify modulators of ecological and evolutionary rates, like

temperature or sensitivity to mutation, which can synchronize or desynchronize ecology and evolution.

We speculate that global change may increase the occurrence of eco-evolution and emergent system

behaviours which represents substantial challenges for prediction. Our perspective represents an attempt

to integrate ecology and evolution across disciplines, from gene-regulatory networks to geomorphology

and across timescales, from contemporary dynamics to deep time.

Introduction

That evolutionary and ecological change can happen on similar timescales has been known since the

mid of the 20th century (Pimentel, 1961; Chitty, 1967; Antonovics, 1976). Interestingly, this “old” idea

has only recently been revived thanks to conceptual advances (e.g., the genotype-phenotype map), long-

term studies and advances in mathematical modelling which have made it operational (Huneman, 2019).

Starting in the early 2000s, eco-evolutionary dynamics and feedbacks, or eco-evolution for short, have

experienced an important hype (Bassar et al., 2021). Accordingly, reviews, perspectives (Fussmann et al.,

2007; Kokko & L´opez-Sepulcre, 2007; Pelletier et al., 2009; Post & Palkovacs, 2009; Lion, 2018), special

issues (BES special issue “Eco-evolutionary dynamics across scales” 2019) and entire books (Hendry,

2017; McPeek, 2017) have been written on the topic. However, one major question keeps coming back:

What is actually an eco-evolutionary interaction?

Hendry (2017) proposes ﬁve categories: the ﬁrst two are deﬁned as eco-evolutionary “dynamics” where

an ecological (evolutionary) change inﬂuences an evolutionary (ecological) change, but not the other way

around. The third and fourth category are “feedbacks” which may be broad sense feedbacks where the

starting and the end point of the feedback need not be identical. Fifth, the core or narrow sense eco-

evolutionary feedback sensu Hendry involves identical starting and end-points. For instance, plant seeds

could exhibit morphological traits that protect them from avian seed predation. This could lead to the

evolution of new beak morphologies in the birds, which may ultimately feed back on plant evolution.

Hendry (2017) also states that all these dynamics should be happening in “contemporary time”. We

would like to note that the word “change” has to be used with caution. As McShea & Brandon (2010)

have argued, the null expectation for a biological system is continuous change rather than permanence.

Variation keeps occurring, so that permanence, like the continued existence of some taxa for millions of

years, is something worth explaining and may require stabilising natural selection as a cause. Therefore,

in the context of eco-evolution we should understand “change” in its most general sense that also includes

permanence, that is, zero change, as a special case.

Bassar et al. (2021) argue that the most correct and useful deﬁnition of eco-evolution is restricted

to Hendry’s broad and narrow sense feedbacks with an emphasis on there being “no separation in time

between ecological and evolutionary dynamics”. They also emphasize the identical ecological and evo-

lutionary timescales implicitly assuming that both are fast. In their view, this is the only case where

truly novel dynamics will emerge that cannot be explained by classical models which, as they write, usu-

ally assume a separation of timescales and weak selection, that is, small phenotypic eﬀects of mutations

(Lion, 2018). This deﬁnition of eco-evolution has led to studies examining the conditions promoting rapid

evolution, such as the genetic architecture of the traits involved (Rudman et al., 2017; Yamamichi, 2022).

But what is “rapid” evolution? And why is ecology considered to be always fast? Timescales sensu

Slobodkin (1961) can be divided into ecological, which comprises time in the 10s of generations, versus

evolutionary, which lies more in the 100,000s of generations. More focused on evolutionary dynamics,

Gingerich (2001, 2009) diﬀerentiates between a generational timescale, which is the most fundamental

timescale, and then microevolutionary and macroevolutionary timescales. Following Gingerich (2001),

micro- and macroevolutionary timescales are timescales of observation and not of the actual process of

evolution which happens on the generational timescale.

One of the emerging challenges is to identify how rapid evolution is relative to ecology in some

pattern of interest, leading to the design of eco-evolutionary partitioning approaches (Hairston et al.,

2005; Collins & Gardner, 2009; Stoks et al., 2015; Govaert et al., 2016). Interestingly, quantiﬁcation of

evolutionary rates showed that these rates tend to be higher than one used to think, especially if measured

on short timescales (Hendry & Kinnison, 1999). All rates can be projected onto the same generation-

to-generation rates if analysed correctly and evolution only seems slow on long timescales, as mentioned

above (Gingerich, 2009). Most recently, DeLong et al. (2016) quantitatively showed, using a dataset

encompassing a wide array of organisms from protozoans to humans, that evolution (rate of phenotypic

change; we here remain on the level of patterns, we will discuss processes below) can be fast, but is usually

slightly slower (by a factor <10) than ecological dynamics (rate of population change). These studies

focus on quantitative changes of phenotypes, but qualitative changes, such as key innovations (Hunter,

1998; Wagner, 2011), might require more fundamental changes in metabolic pathways or the bodyplan,

and occur less frequently, especially if historical contingencies are involved (Blount et al., 2008). One

may therefore again distinguish between two evolutionary timescales, more or less coinciding with the

classical micro- vs. macroevolutionary diﬀerentiation.

Most of the work we have discussed so far on eco-evolution has a strong background in evolution-

ary biology and inﬂuences from functional or ecosystem ecology seem weak. This lack of synthesis is

apparent in Hendry (2017)’s book, for example, and clearly biases the existing work and hinders a full

integration of ecology and evolution. While this was already noted over 10 years ago (Matthews et al.,

2011), limited progress seems to have been made (for exceptions, see Kylaﬁs & Loreau, 2008; Bassar

et al., 2010; El-Sabaawi et al., 2014; Matthews et al., 2016). Most often, ecology, i.e., the environment,

serves as a “theatre” for the gene-centred “evolutionary play” (Hutchinson, 1965) because ecology and

evolution have more or less divorced since Darwin, and the Modern Synthesis had little interest in ecology

(Huneman, 2019). Even the “ecological genetics” school (Whitham et al., 2006) was not really interested

in ecology, and no eco-evolutionary feedbacks were envisaged. Furthermore, ecology is often understood

as, or reduced to, pure demography. This focus is obvious apparent in current eco-evolutionary analyses

conducted by evolutionary biologists, beginning with Pimentel (1961) and Chitty (1967). Conversely,

it also seems that functional ecologists have had little interest in evolutionary processes (Loreau, 2010;

Huneman, 2019).

If we want to take a more ecosystem-level perspective, we must ask whether ﬂuxes of matter and

energy, both in trophic networks and the physical environment (Corenblit et al., 2009), may also play a role

in eco-evolution. This implies that we need to understand on which timescales such ﬂuxes happen. Using

the meta-ecosystem ecology framework, Gounand et al. (2018b) have summarized available information

for carbon ﬂuxes, and show that ﬂuxes vary widely and across orders of magnitude. Yet, often, timescales

are within years, implying that ecosystem dynamics and demographic rates are comparable, and might

even be intrinsically linked. Interestingly, spatial ﬂows of matter and energy are often mediated by spatial

behaviour of organisms (movement, foraging, seasonal migrations, dispersal; Gounand et al., 2018a) which

provides a mechanistic link between metacommunity and metaecosystem ecology (Loreau et al., 2003;

Massol et al., 2011b). This behavioural link is especially true for taxonomically similar ecosystems (e.g.,

two lake ecosystems) that are more linked by dispersal than ecosystems that are biotically dissimilar (e.g.,

terrestrial-aquatic linkages) which may be more linked by ﬂows of resources (Gounand et al., 2018a). Of

course, diﬀerent organisms within an ecosystem may experience diﬀerent timescales, such as bacteria

versus large mammals. While interesting and potentially relevant for ecosystem dynamics this is beyond

the scope of the current article.

At a more fundamental level, the abiotic environment is deﬁned by the geological and geomorpho-

logical settings that impact abiotic ecosystem properties (e.g., via physico-chemical conditions, leaching

of nutrients, ﬂuxes and organization of mineral matter) and also impact the biotic component because

geology and geomorphology provide the environmental matrix in which (meta)ecosystem dynamics play

out (Phillips, 2021). In systems in which geology and geomorphology are the “pacemakers”, ecological

dynamics will occur at much longer timescales than demography.

Given the central role of timescales and lack of true integration of ecology and evolution, we here

propose to conceptualize eco-evolution within a two-dimensional time space. At the extremes of this

time space we can identity four system states (Fig. 1): A) fast eco-evolution sensu Bassar et al. (2021)

where evolution is fast enough to impact fast ecology (demography); B) classical ecology and evolutionary

ecology, where evolution is too slow to immediately impact fast ecological dynamics. Note that even if the

ecological dynamics results from past evolutionary changes (and vice versa), the timescales do not match;

C) evolution is faster than ecology which could imply rapid adaptation to relatively slower environmental

changes (rapid adaptation to anthropogenic disturbance Chakravarti & van Oppen, 2018; Lagerstrom

et al., 2022) and, ultimately, neutral evolutionary dynamics; and ﬁnally D) both are slow such as when

geomorphological conditions provide an ecological opportunity for a rare key innovation which then feeds

back and impacts geomorphology (Corenblit et al., 2011; Butterﬁeld, 2017; Pausas & Bond, 2022). We

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Eco-evolutionfromdeeptimetocontemporarydynamics:theroleoftimescalesandratemodulatorsEmanuelA.Fronhofer1,DovCorenblit2;3,JhelamN.Deshpande1,LynnGovaert4,PhilippeHuneman5,FrederiqueViard1,PhilippeJarne6andSaraPuijalon71.ISEM,UniversitedeMontpellier,CNRS,IRD,EPHE,Montpellier,France2.UniversiteClerm...

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