1How Individualized Niches Arise: Defining Mechanisms of Niche
2Construction, Niche Choice and Niche Conformance
3Rose Trappes*, Behzad Nematipour*, Marie I. Kaiser*, Ulrich Krohs*, Koen J. van
4Benthem^, Ulrich R. Ernst^, Jürgen Gadau^, Peter Korsten^, Joachim Kurtz^, Holger
5Schielzeth^, Tim Schmoll^, Elina Takola^
6 7*Shared first authorship 8^Equal contribution 9 10Affiliations
11RT, MK: Department of Philosophy, Bielefeld University, Universitätsstr. 25, 33615 12Bielefeld, Germany 13BN: Center for Philosophy of Science, University of Münster, Domplatz 23, 48143 Münster, 14Germany 15UK: Department of Philosophy, University of Münster, Domplatz 23, 48143 Münster, 16Germany 17KvB: Department of Theoretical Biology, Bielefeld University, Universitätsstr. 25, 33615 18Bielefeld, Germany 19UE, JG, JK: Institute for Evolution and Biodiversity, University of Münster, Hüfferstraße 1, 2048149 Münster, Germany 21PK: Department of Animal Behaviour, Bielefeld University, Konsequenz 45, 33615 22Bielefeld, Germany 23TS: Department of Evolutionary Biology, Bielefeld University, Konsequenz 45, 33615 24Bielefeld, Germany 25HS, ET: Population Ecology Group, Institute of Ecology and Evolution, Friedrich Schiller 26University Jena, Dornburger Straße 159, 07743 Jena, Germany 27
28ORCiD 29RT: 0000-0002-6398-5404 30BN: - 31MIK: 0000-0002-9307-7474 32UK: - 33KvB: 0000-0002-3841-2110 34UE: 0000-0002-6330-5341 35JG: 0000-0003-1258-5379 36PK: 0000-0003-0814-9099 37JK: 0000-0002-7258-459X
1 38HS: 0000-0002-9124-2261 39TS: 0000-0003-3234-7335 40ET: 0000-0003-1268-5513 41
42Correspondence
43Rose Trappes, [email protected]
44
45Author Contribution Statement
46All authors conceived the theoretical framework. RT, BN, MK & UK created the initial draft
47and performed revisions of the manuscript. KvB, UE, JG, PK, JK, HS, TS & ET contributed
48examples and helped to revise the text and figures. All authors approved the submitted
49version.
50
51Funding
52This research was funded by the German Research Foundation (DFG) as part of the SFB
53TRR 212 (NC³) – Project number 316099922.
54
55Acknowledgements
56We would like to acknowledge Caroline Müller, Oliver Krüger, and Norbert Sachser for
57generating the initial framework of the NC3 mechanisms which we develop and present here,
58and for helpful comments during writing. Thanks are also due to all members of the CRC
59TRR-212 at the University of Münster, Bielefeld University and Jena University and to the
60philosophers of biology at Bielefeld University for their attention and constructive feedback
61on the project.
2 62How Individualized Niches Arise: Defining Mechanisms of Niche Construction, Niche
63Choice and Niche Conformance
64
65Abstract
66The debate between the extended evolutionary synthesis (EES) and the modern synthesis
67(MS) partly relies on different interpretations of niche construction. We dissect the umbrella
68term of niche construction into three separate mechanisms: niche construction (taken in a
69narrow sense), in which individuals make changes to the environment; niche choice, in which
70individuals select an environment; and niche conformance, in which individuals change their
71phenotypes. Each of these individual-level mechanisms affects an individual’s phenotype-
72environment match, its fitness, and its individualized niche, defined in terms of the
73environmental conditions under which an individual can survive and reproduce. Our
74conceptual framework distinguishes several ways in which individuals alter the selective
75regimes that they and other organisms experience. It also places clear emphasis on individual
76differences and construes niche construction and other processes as evolved mechanisms. We
77therefore argue that our framework helps to resolve the tensions between EES and MS.
78
79Keywords: extended evolutionary synthesis, niche construction, individualized niche,
80individual differences, phenotypic plasticity
81
82Introduction
83Organisms change their environment—beavers build dams, birds build nests, earthworms
84alter soil structure. It seems uncontentious that these organisms thereby modify their living
85conditions and the selective regime under which they live. Under dispute, however, is what
86these modificatory actions, often called niche construction, mean for evolutionary theory.
3 87One view is that through modifying the environment organisms actively influence the
88evolution of their own and other species, making organisms not just objects of, but subjects in
89evolution (Lewontin 1983, Laland et al. 2015). This view is central to the Extended
90Evolutionary Synthesis (EES). Another view interprets organisms’ modificatory actions as
91adaptations that are the outcome of earlier stages of evolution. This classical view of the
92Modern Synthesis (MS), in contrast to EES, therefore maintains organisms’ status as mere
93objects of evolutionary processes, with environmental modifications understood as a result of
94evolution by natural selection (Dawkins 1982).
95The dispute might look like a chicken and egg problem—which came first, selection or
96construction? But there is far more at stake than just where to put the focus in a sequence of
97alternating steps. EES and MS have starkly contrasting understandings of evolution and take
98different biological disciplines as relevant for evolutionary theory. EES considers organismal
99activities as dependent on modifications in developmental processes, which in turn affect
100evolution (Laland et al. 2014). It thus demands an extension of MS by, for instance,
101integrating developmental and behavioral biology. In contrast, contemporary interpretations
102of MS acknowledge developmental processes and interactions between the genotype and the
103environment, yet claim that these can be accommodated within the classical framework that
104sees genetic change as the core of evolutionary change (Wray et al. 2014).
105We believe that the alleged incompatibility of EES and MS accounts of niche construction
106can be partly resolved. We argue for recognizing the different ways in which organisms alter
107their environment and their relation to the environment as a set of evolved causal mechanisms
108that play a role in evolutionary processes. This insight derives from our interdisciplinary
109work within the Research Consortium “A Novel Synthesis of Individualisation across
110Behaviour, Ecology and Evolution: Niche Choice, Niche Conformance and Niche
111Construction (NC3)” (https://www.uni-bielefeld.de/biologie/crc212). In this paper, we
4 112undertake some conceptual clarifications that help to diminish the perceived conflict between
113EES and MS. We do so largely with a focus on animals, but we see our framework as
114applicable to plants and other taxa.
115We first point out that niche construction is carried out by individuals and that there can be
116individual differences in niche construction (section 1). We subdivide the umbrella concept
117of niche construction into three distinct mechanisms through which individuals interact with
118their environments: making changes to the environment (niche construction in the narrow
119sense), selecting an environment (niche choice), and altering their phenotype in response to
120the environment (niche conformance) (sections 2 and 3). All three mechanisms alter the
121phenotype-environment match and the individual’s fitness, thereby determining the
122ecological niche of an individual, defined as the set of environmental conditions in which an
123individual can survive and reproduce (section 4). Hence, we refer to these mechanisms as
124“niche-altering mechanisms” or “NC3 mechanisms”. Finally, we discuss which aspects of the
125debate about the evolutionary relevance of niche construction can be resolved by our
126conceptual work, which ones become empirical questions, and which ones remain as
127differences between different framings of evolution (section 5).
128
1291. Individual Differences in Niche Construction
130We can start with a classical example of niche construction: “Birds build nests” or more
131concretely, “Common buzzards (Buteo buteo) build nests with twigs from various tree
132species.” Here, niche construction might be understood at the species level, describing what
133nest-building behavior is characteristic of the species B. buteo. Yet in the end it is individual
134buzzards that build nests in the environment. In fact, niche construction activities always
135require the action of individuals (sometimes in pairs or groups) that change the environment.
5 136According to the EES, these individual activities can in turn affect the evolutionary
137trajectories of populations and species.
138The relation between individual activities and species evolution is sometimes obscured in
139definitions of niche construction. For instance, Lewontin and Levins first described niche
140construction—prior to the coining of the term—as such: “the organism influences its own
141evolution, by being both the object of natural selection and the creator of the conditions of
142that selection” (Lewontin and Levins 1985, p. 106). Here “the organism” is at once
143population or species—since it has its “own” evolution, and it is populations and species
144which evolve—and individual—performing activities that alter the conditions of selection.
145Later definitions of niche construction try to avoid this equivocation. For instance, Odling-
146Smee, Laland and Feldman caution that “niche construction is typically expressed by
147individual organisms, but natural selection is a process that operates within populations”
148(Odling-Smee et al. 2003, pp. 41-42). In other words, it is not the niche-constructing
149individuals themselves that evolve, but their population or species.
150Recognizing individuals as the agents of niche construction invites consideration of an often-
151overlooked aspect of niche construction: individual differences. Not all individuals in a
152population are the same, and different individuals can construct niches in different ways.
153These individual differences in niche construction are important because they can have
154evolutionary consequences.
155For instance, queens of the California Harvester Ant (Pogonomyrmex californicus) vary in
156their colony founding behavior, either tolerating other queens or killing them (Rissing et al.
1572000, Clark and Fewell 2014). This individual difference leads to fundamentally different
158social structures with either multiple unrelated queens or a single queen (Overson et al.
1592014). The proportion of multiple and single queen societies varies substantially between
6 160subpopulations (Overson et al. 2016). It seems that colony density, degree of territoriality or
161aggression and resource availability (Haney and Fewell 2018) are crucial components of the
162selective environment that favors either one or the other type of niche construction.
163Being clear that we are talking about individual activities invites us to focus on a particular
164sort of niche, namely the individualized niche. The idea that individuals have their own,
165individualized niches has been proposed following the recognition of ecological
166specialization within populations (Roughgarden 1972, Bolnick et al. 2003, Dall et al. 2012,
167Violle et al. 2012). The population niche concerns the conditions under which a population as
168a whole persists; it does not take into account that some individuals might be better off under
169conditions that are less favorable for others. In contrast, the individualized niche concerns
170how the requirements and dispositions of an individual relate to its environment. Individuals
171that differ from each other will be confronted, in the very same environment, with different
172impact or effects of the environmental conditions, consume different resources, have different
173interactions with conspecifics, and so on, and these interactions can have different fitness
174effects. We summarize our definitions of species and individualized niches in BOX 1 and
175explain them in detail in section 4.2.
7 BOX 1. The ecological niche of an individual The ecological niche of a species is the set of environmental conditions under which it exists and can maintain itself (implying non-negative population growth rates in the long run).
We define the fundamental individualized niche as the range of environmental conditions under which a specific individual with a given set of traits could possibly live and reproduce.
We define the realized individualized niche as the environmental conditions under which a specific individual does actually live and reproduce. The realized niche is thus the subset of the fundamental niche realized in the actual environment in which an individual lives.
We emphasize the dynamic nature of individualized niches. A fundamental individualized niche can change by the individual’s activities that alter its physiological or behavioral phenotypes or developmental pathways. A realized individualized niche can change by activities that alter the experienced environment of an individual, and by environmental changes. 176
177Individual organisms engage in many sorts of activities altering their individualized niches.
178Most of the classical examples of niche construction involve organisms actively making
179changes to their environments, rather than, for instance, changing the environmental
180conditions they live in by relocation. This makes sense, because we intuitively understand
181niche construction in analogy to human construction of artifacts like buildings or roads
182(Archetti 2015).
183However, many niche construction theorists understand niche construction more broadly.
184Odling-Smee, Laland and Feldman (2003) include relocating as an instance of niche
185construction. Others include phenotypic alteration that changes how an environment is
186experienced as a kind of niche construction (Lewontin and Levins 1985, Aaby and Ramsey
1872019). The use of “niche construction” to cover such diverse phenomena can be confusing,
188especially given that paradigmatic examples continue to revolve around making changes to
189the environment.
8 190We therefore restrict the concept of niche construction to what we see as its intuitive scope:
191organisms making changes to their environment. To refer to other ways in which individuals
192interact with their environment and thereby alter their niches, we employ two additional
193terms: niche choice occurs when individuals select an environment, and niche conformance
194occurs when individuals alter their phenotype in response to the environment (see also
195Edelaar and Bolnick 2019). Collectively, we refer to niche construction, niche choice, and
196niche conformance as niche-altering mechanisms, or “NC3 mechanisms”.
197
1982. Introducing the NC3 Mechanisms
199NC3 mechanisms consist of entities and activities that are spatially, temporally and
200hierarchically organized in specific ways, and produce a phenomenon. This accords with
201definitions of mechanisms as put forward in philosophy of science (Bechtel and Richardson
2021993, Glennan 1996, 2017, Machamer et al. 2000, Craver and Darden 2013). The activities
203that individuals carry out lead to a specific outcome: a change in the phenotype-environment
204match and in the individual’s fitness, and an individualized niche (section 4). Referring to
205niche construction, niche choice and niche conformance as three mechanisms highlights that
206we seek to understand the causal process of how match, fitness and individualized niches
207change.
208NC3 mechanisms share a general structure. Usually, they are organized around a focal
209individual. The focal individual, sometimes in cooperation with other individuals, is engaged
210in a focal activity. The philosophical term ‘activity’ is similar to the term ‘behavior’ in that it
211also includes changes such as reducing locomotion or going to sleep. In other words,
212activities are what organisms do. Activities can involve one or more entities; entities involved
213in an activity can be active, performing the activity, or they can be passive, having the
9 214activity done to them (Machamer et al. 2000, Illari and Williamson 2013, Kaiser 2018). For
215example, blood parasites are actively involved in the activity ‘infecting’, whereas buzzard
216chicks as hosts have a passive role in this activity. Similarly, beavers are actively involved in
217the activity ‘cutting trees’, whereas trees are passively involved in this activity. For the NC3
218mechanisms, the focal individual is actively involved in the focal activities.
219The different NC3 mechanism are discerned by the respective focal activity. In the case of
220niche construction, the focal activity is to make changes to the environment, in niche choice
221the focal activity is to select an environment and in niche conformance the focal activity is to
222change the phenotype in response to the environment (Figure 1). These focal activities are
223quite abstract; in descriptions of concrete NC3 mechanisms they are replaced by more specific
224activities involving the focal individual, other organisms and abiotic factors (Kaiser and
225Trappes forthcoming). In the example of harvester ants, for instance, the niche construction
226activities involve aggressive or tolerant interactions as well as performing certain colony
227founding tasks.
228
229Figure 1. NC3 mechanisms. (a) Three individuals, A, B and C are in the same environment.
230Each individual uses a different NC3 mechanism to change its phenotype-environment match.
231(b) Each NC3 mechanism involves a different focal activity. Focal individuals A, B and C can
10 232make changes to the environment, select the environment, or adjust the phenotype in
233response to the environment. (b) is modified from Kaiser and Trappes (in press).
234
235The outcome of NC3 mechanisms, the phenomenon they produce, can also be characterized
236on a general level. NC3 mechanisms change the match between the focal individual’s
237phenotype and its environment, as well as the individual’s fitness, understood as the number
238of offspring produced or its contribution to the gene pool of future generations (more in
239section 4.1). Consequently, NC3 mechanisms also change an individual’s niche, taken
240preliminarily as the set of environmental parameter values under which it survives and
241reproduces (BOX 1). This is why we refer to the three focal activities (‘making changes to’
242environment, ‘selecting’ environment, and ‘changing’ phenotype in response to the
243environment) as niche-altering activities. It is important to note that the NC3 mechanisms
244refer not to a choice of, conformance to or construction of the niche but rather to a choice of,
245conformance to or construction of the environment, which in turn affects the niche.
246BOX 2 summarizes the general structure of NC3 mechanisms. The general structure together
247with the distinction of the three focal activities gives rise to definitions for the three NC3
248mechanisms.
11 BOX 2. The Focal Activities of NC3 Mechanisms In NC3 mechanisms, a focal individual is actively involved in a focal activity, which leads to a change of the phenotype-environment match, a fitness change, and a change of the individualized niche. Niche Construction is the mechanism by which an individual makes changes to its environment, resulting in a change of the individual’s phenotype-environment match, fitness and individualized niche.
Niche Choice is the mechanism by which an individual selects an environment, resulting in a change of the individual’s phenotype-environment match, fitness and individualized niche.
Niche Conformance is the mechanism by which an individual changes its phenotype, resulting in a change of the individual’s phenotype-environment match, fitness and individualized niche. 249
250
251The NC3 mechanisms do not always appear separately. Often, two or even all three
252mechanisms will occur simultaneously or in sequence. For instance, a buzzard building a nest
253is certainly a case of niche construction, but buzzards often need to relocate to a suitable
254habitat and choose a tree in which to build their nest, so that niche choice precedes niche
255construction.
256In addition, the very general nature of the NC3 mechanism definitions in combination with
257the fact that mechanisms can occur together means that classification can be ambiguous in
258some cases. For instance, an organism making changes to the environment (niche
259construction) typically involves certain behavioral or other phenotypic changes, as occurs in
260niche conformance. Similarly, choosing a specific social group (niche choice) will also
261induce changes in the social dynamics of that group, as occurs in niche construction. Each
262case must therefore be considered carefully in light of the mechanisms at play, and there may
263be borderline cases that are difficult to categorize.
12 264In the next section we analyze the three focal activities in more detail and provide some
265examples. Later, we tackle the other elements of the definitions: the way individual activities
266lead to changes in organism-environment match and fitness, and their effects on
267individualized niches (section 4).
268
2693. Three Types of Niche-Altering Activities
2703.1 Rebuilding the Environment: Niche Construction
271Mechanisms of niche construction are characterized by the focal individual actively making
272changes to its environment. The classic examples of niche construction cited earlier—beavers
273building dams, birds building nests, and worms altering soil structure—involve focal
274individuals altering the properties of their abiotic environment. However, individuals can also
275make changes to their biotic environment through interactions with organisms from other
276species or with conspecifics.
277A special case is when individuals change their social environment, for instance by altering
278the way conspecifics behave by interacting with them. For example, in cooperatively
279breeding meerkats (Suricata suricatta), dominant females show increased aggression towards
280pregnant subordinate females, resulting in their temporary eviction from the social group.
281Being evicted induces severe stress in the subordinates, causing spontaneous abortions. In
282this way, dominant females suppress competitors’ reproduction, thereby monopolizing
283reproduction in the group (Young et al. 2006).
284An interaction with other organisms or the abiotic environment must satisfy two conditions to
285count as the focal activity in niche construction. First, there must be a change in the
286environment and not just a change in which environment the individual relates to, which
287would be choice. Second, the focal individual must have an active role (see above, Section 2).
13 288This excludes changes in the environment in which an individual is only passively involved,
289such as changes in a non-human organism’s environment produced by human activities such
290as farming or anthropogenic climate change. On the other hand, activities such as defecation
291or trampling can count as niche construction since the focal individual is actively engaging in
292activities that change their environment, as long as the focal individual’s phenotype-
293environment match and fitness also change as a result. These two conditions are captured in
294our definition (BOX 2) by the phrase ‘makes changes to its environment.’
295
2963.2 Selecting the Environment: Niche Choice
297The second NC3 mechanism is niche choice, in which the focal individual selects the
298environment with which it interacts. In cases of niche choice individuals change how they
299interact with different parts of the environment, rather than changing their phenotype (niche
300conformance) or making changes to the environment (niche construction).
301A paradigmatic type of niche choice is an individual moving to a different habitat. Sometimes
302this is a temporary or context dependent choice. For instance, in azure sand grasshoppers
303(Sphingonotus azurescens), darker individuals prefer darker underground, whereas
304individuals with lighter colors prefer lighter underground. Interestingly, manipulation of
305individuals’ color (with dark or light paint) led to changes in preferences such that dark-
306painted individuals preferred darker underground, independent of their original, natural
307coloration (Camacho et al. 2020). An example of a more permanent niche choice is territory
308establishment. For instance, movement data from juvenile black grouse (Tetrao tetrix)
309showed that, following natal dispersal during the first year, most individuals remained in the
310areas where they spent their first winter (Caizergues and Ellison 2002).
14 311Niche choice does not necessarily involve physical relocation but can include selective
312interactions with parts of the environment, especially through choice of resources or social
313groups. An illustrative example of individual differences in the choice of the social
314environment is provided by work on cliff swallows (Petrochelidon pyrrhonota), a colonial
315bird, where individuals have heritable preferences for breeding in smaller or larger groups
316(Brown and Brown 2000). Another example is the California harvester ants referred to in
317section 1, where queens choose whether to found a nest together with other queens.
318In most cases of niche choice, the focal individual changes its location, resource use or
319interactions with its (social) environment. But what about an individual choosing to not
320change anything? We think that these cases should be counted as niche choice if the
321individual was able to explore different options of changing its relation to the environment.
322Even if this exploration does not result in a change of the individual-environment relation, it
323does involve individuals actively approving their present environments. It might be difficult
324to discern such cases empirically from cases where an individual does not make a choice
325(because it does not explore different environmental options). However, there is a conceptual
326delineation of the cases. It is an interesting empirical question whether maintaining the same
327relation to the environment is or is not the result of engaging in a choice procedure.
328
3293.3 Adjusting the Phenotype: Niche Conformance
330The third NC3 mechanism is niche conformance, which involves focal individuals changing
331their phenotypes in response to environmental conditions. Niche conformance involves
332phenotypic plasticity, which is the capacity of an organism to develop distinct phenotypes in
333response to environmental variation (Pigliucci 2001, 2005). Accordingly, the focal activity of
15 334changing the phenotype that characterizes niche conformance (BOX 2) can also be described
335as adjusting the phenotype in response to certain environmental conditions.
336Yet niche conformance involves more than just the focal activity. Unlike phenotypic
337plasticity, niche conformance also includes how phenotypic adjustment leads to changes in
338the phenotype-environment match, fitness, and the individualized niche of the focal
339individual (section 4). In particular, by stressing inter-individual variation of organisms in
340their plastic responses, so-called individual-by-environment interactions (Nussey et al. 2007),
341it directly leads to an expectation that the resulting niches are individualized (section 4.2).
342Niche conformance may accommodate any kind of trait (morphological, physiological,
343behavioral or life history) and can be applied to irreversible developmental changes during an
344individual’s lifetime (non-labile traits) as well as to reversible changes in response to the
345current environment (labile traits). An example for a non-labile, morphological trait is the
346expression of inducible defenses like spines and helmets by water fleas (e.g., Daphnia
347cucullata) during development in response to anticipated variation in predation risk (Laforsch
348and Tollrian 2004). An example for a labile, life-history trait is the timing of reproduction in
349many temperate bird species where individual females track between-year variation in spring
350temperatures in order to match supply and demand in nestling food (Charmantier et al. 2008).
351Another example is provided by Macrostomum hystrix, a flatworm, in which individuals are
352facultative selfers that reproduce through outcrossing when a mating partner is available, but
353self-fertilize if no partner has been available for a certain amount of time (Ramm et al. 2012).
16 3544. NC3 Mechanisms Affect Phenotype-Environment Match, Fitness, and the
355Individualized Niche
3564.1 Phenotype-Environment Match and Fitness
357Each of the NC3 mechanisms brings about a change in the phenotype-environment match and
358in fitness. The notion of match that we use is evaluative, referring to how well an organism’s
359phenotype matches to its environment. Match is often measured by reproductive success. In
360this case, match and fitness are positively correlated. Match can also be measured using other
361measures such as food uptake rate, body condition, efficiency of locomotion, or effectiveness
362of coloration (e.g., camouflage, aposematic warning colors). Non-fitness measures of match
363may still lead to a correlation between match and fitness, since an improvement of factors
364like body condition or effective mimicry will often increase an organism’s fitness.
365It might seem natural to think that NC3 mechanisms would not just affect but also improve
366match and fitness of the focal individual. We decided not to restrict the definitions of the NC3
367mechanisms to cases which improve match and increase fitness. There are two main reasons
368for this decision.
369First, requiring that NC3 mechanisms increase fitness would mean that a specific mechanism
370would not count as an NC3 mechanism when, due to some intervening factor, the overall
371outcome is less advantageous for the focal individual. Second, we define fitness as absolute
372fitness in line with Hutchinson’s population level growth rate (Section 4.2). However, at the
373level of individuals even a decrease in absolute fitness could nevertheless be beneficial in
374evolutionary terms if it increases relative fitness. This would be the case if for instance
375conspecifics suffer more from the operation of an NC3 mechanism than the focal individual.
376Thus, the fitness effects of NC3 mechanisms may depend on the specific environment, in
377particular on social conditions. Fluctuating conditions can thus lead to a change of the sign of
17 378the fitness outcome. It is for such reasons that we believe NC3 mechanisms should also allow
379for instances of an activity decreasing individual fitness or other measures of match. Such
380cases can be particularly relevant to study, since they can illuminate why individuals engage
381in apparently non-adaptive activities. In general, however, we expect that evolved NC3
382mechanisms will tend to increase individuals’ (absolute and relative) fitness (Odling-Smee et
383al. 2003, p. 48), since the mechanisms would otherwise have been selected against. This
384assumption is reflected in many empirical studies that investigate the adaptive value of NC3
385mechanisms.
386
3874.2 Individualized Niches
388So far, we have addressed individual activities and their consequences for match and fitness.
389The last element of the NC3 mechanisms is their effect on individualized niches. We
390understand the individualized niche as the individual-level counterpart of the Hutchinsonian
391population niche (Hutchinson 1957, Holt 2009). Re-defining Hutchinson’s concept at the
392individual level requires several modifications.
393First, Hutchinson defines the niche in terms of the environmental conditions under which a
394population could persist indefinitely, a condition that needs some modification to be
395transferable to the case of individuals with limited life spans. We define the limits of the
396individualized niche in terms of individual realized fitness equal to or greater than what is
397necessary for the individual to replace itself in future generations (i.e., each individual
398leaving one reproducing offspring). In addition, in the context of the NC3 mechanisms, we are
399interested in how exposure to different environmental parameters can change fitness above
400the minimum required for replacement. We thus need to consider gradual fitness values for
401different subsections of the niche, as Hutchinson proposed for population niches (Hutchinson
18 4021957). The individualized niche is the mapping, or function, of fitness over sets of
403environmental parameters.
404Second, to accommodate changes of niche relations within a lifetime, the quality of match
405needs to be evaluated with respect to a given situation or short period of time. Realized
406fitness, being a lifetime outcome, is not the appropriate parameter. Instead, fitness proxies
407such as individual (ontogenetic) growth rate, survival across life stages, territory possession,
408mating rates and fertilization success can serve as indicators of the quality of a combination
409of niche parameter values for an individual at a given time.
410Third, we need to distinguish between the fundamental niche as a set of possibilities and the
411realized niche as the actualization of one of these possibilities (BOX 1). We define a
412fundamental individualized niche as the environmental conditions under which an individual
413could possibly live and reproduce. An individualized realization of a niche is in turn the
414subset or region of the fundamental niche realized by the environmental conditions under
415which the individual actually survives and reproduces. We call this a realized individualized
416niche, even though this does not exactly mirror Hutchinson’s concept of a realized niche. In
417the next section, we discuss how the NC3 mechanisms change individualized niches and how
418they affect fundamental and realized individualized niches differently.
419
4204.3 NC3 Mechanisms Alter Individualized Niches
421Individuals conform to, choose or construct the environment rather than the niche. Yet these
422activities do result in changes of the individualized niche (Figure 2).
19 423
424Figure 2. NC3 mechanisms produce changes in the individualized niche. Simplified
425individualized niches, showing two possible phenotypes and their values for a fitness or
426match (e.g., growth rate, fertilization success, performance) along a single niche dimension
427(e.g., temperature, food abundance). (a) Niche construction: an individual with phenotype P
428in environment 1 makes changes to its environment so that it becomes environment 2,
429thereby increasing the individual’s fitness. (b) Niche choice: an individual with phenotype P
430in environment 1 selects environment 3, thereby increasing its fitness. (c) Niche
431conformance: an individual with phenotype P in environment 1 adjusts to phenotype Q,
432thereby increasing its fitness within environment 1.
433
434Niche construction can produce a change in the values of environmental factors such as
435temperature, humidity, resource availability, or population density. The set of these values is
436equivalent to a certain point or region in the fundamental individualized niche. Since niche
437construction affects which set of niche parameters is realized in the environment of the
438individual, niche construction changes the realized individualized niche.
20 439As niche construction changes the selective regime, it might also lead to an evolutionary
440response. If phenotypic variation is at least partly heritable, then natural selection may change
441the phenotypes of future individuals; phenotypic change through natural selection could in
442turn alter the fundamental individualized niches of future individuals. For example, most bird
443species construct elaborate nests where eggs are incubated and chicks raised until fledging
444(Hansell 2000, Mainwaring et al. 2014). Variation in nest construction among breeding
445individuals or pairs influences the nest’s insulating properties and thereby the
446microenvironment experienced by the parents and their offspring (Mainwaring 2017), which
447can facilitate natural selection on phenotypes, potentially leading to evolutionary changes in
448both nest-building and temperature tolerance (again, assuming such phenotypic variation is
449heritable).
450The consequences of niche choice for the realized individualized niche are the same as for
451niche construction, but they are brought about by selecting a different environment instead of
452modifying the existing environment (Figure 2). Individual differences in choice driven by
453factors such as physiology, morphology or social dynamics can lead to individuals realizing
454different niches. For instance, in the invasive racer goby (Babka gymnotrachelus),
455intraspecific interactions drive dispersal, as subordinate individuals tend to move greater
456distances in search of resources and less hostile social environments (Grabowska et al. 2019).
457Niche conformance changes the individual’s phenotype. A different phenotype means that the
458organism can, for instance, tolerate different conditions or perform better on different
459resources. This in turn means that the individual will have changed its fitness value given one
460and the same set of niche parameter values. In addition, there may be different sets of
461environmental conditions under which the individual can survive and reproduce. In both
462instances, the fundamental individualized niche changes, either in which sets of niche
21 463parameter values it includes or in the shape of the fitness function across the ecological
464dimensions of the niche.
465Interestingly, when niche choice or construction induce niche conformance, a change in the
466realized individualized niche (by choice or construction) can eventuate in a change in the
467fundamental individualized niche. For example, individual oystercatchers specializing on
468either soft or hard prey types grow different bill shapes that facilitate efficient processing of
469their specific prey of choice (van de Pol et al. 2010). In this case, birds specializing on a
470particular resource (niche choice) adjust their phenotype (niche conformance) and thereby
471alter not only their realized but also, by altering their performance on different resources and
472thus the fitness function over the resources, their fundamental individualized niche.
473
4745. NC3 Mechanisms and Evolutionary Syntheses
475We began with the conflict between MS and EES. The evolutionary relevance of niche
476construction (in the wide sense, including all three NC3 mechanisms) forms a core point of
477difference between these schools. Our conception of the NC3 mechanisms as ecological and
478evolutionary mechanisms combines aspects from both schools and thus allows for a full
479acknowledgment of niche construction, as discussed in EES, without being in conflict with
480MS.
481Our take on the NC3 mechanisms accords largely with MS. Like proponents of MS, we think
482it is important to assess fitness consequences as they are relevant to long-term evolutionary
483process. We further assume that NC3 mechanisms have an evolutionary history and are
484suitably analyzed as adaptations to environmental conditions in the past (which may or may
485not correspond to current conditions).
22 486We nevertheless initiate a change in perspective, amending the population centered view of
487MS by focusing on individual activities, individual-level mechanisms and the individualized
488niche. We thereby take up the initiative from EES to analyze evolutionary processes on the
489level of individual activities, acknowledging their status as subjects that have an active role in
490evolution. Our focus on mechanisms that comprise a focal individual and its focal activity
491stresses the importance of individuals’ activities (including developmental processes) as
492modulators of the selective regime under which individuals live. We allow for novel activities
493arising by developmental processes that do not have a history of adaptation and may still be
494relevant to phenotype-environment matches, as it is put forward in EES (West-Eberhard
4952003).
496Both MS and EES are therefore embraced by our approach without internal conflict. We
497believe that this shows that the divide between MS and EES is not in all regards
498insurmountable. But our change in perspective does not propose a general answer to the
499question of whether organisms are subjects rather than mere objects of evolution. Instead, it
500invites solving this question empirically rather than dogmatically. Whether an individual’s
501activity drives evolution in a new direction does not depend on subscribing to a theoretical
502framework. It is rather something that can and should be studied empirically.
503We do not deny that crucial differences between MS and EES remain. The general focus of
504EES on the subject status of organisms in evolution will hardly be reconcilable with the gene-
505centered view of MS, even when MS can incorporate the subject view in empirically well-
506supported cases. On the other hand, the role of fitness in MS and the MS perspective on the
507fitness principle (Krohs 2006) are incompatible with the aim of EES to investigate
508evolutionary mechanisms without preconceptions about the way in which they drive
509evolution. There may be good reasons why the debate between MS and EES proponents is
23 510sometimes heated. Part of the debate can nevertheless be transformed into a constructive
511exchange and even partially resolved.
5126. Conclusions
513Organisms modify their niches in a number of different ways. We distinguish three different
514mechanisms by which individuals alter their niches: niche construction, niche choice, and
515niche conformance. The three mechanisms are distinguished by the focal activity performed
516by the focal individual. In niche construction the individual makes changes to the
517environment, in niche choice it selects an environment, and in niche conformance it adjusts
518its phenotype in response to the environment. All of the NC3 mechanisms change individuals’
519phenotype-environment match and their fitness. Because many NC3 mechanisms have
520evolved and persisted through natural selection, we expect them to generally improve
521phenotype-environment match and fitness.
522One interesting feature of NC3 mechanisms is the way they alter individualized niches. Niche
523construction and niche choice affect the realized niche, altering which possibilities of the
524fundamental individualized niche are realized in the environment the individual experiences.
525In contrast, niche conformance affects the fundamental niche, either changing the conditions
526under which the individual can survive and reproduce or affecting the individual’s
527performance on a given range of conditions. Because they are individual-level mechanisms
528which produce individualized niches, NC3 mechanisms highlight the potential for individual
529differences to affect how organisms alter their niches.
530Our framework recognizes the insights of EES that individuals are subjects of evolution,
531affecting the selective pressures to which they are exposed and the resources and information
532available for generating new behavioral variation. In addition, it accommodates approaches
24 533from MS by providing new material for understanding the evolution of niche-altering
534individual activities through natural selection.
535
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