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Coevolution occurs when species interact to influence one another's fitness, resulting in reciprocal evolutionary change. In many coevolving lineages, trait expression in one species is modified by the genotypes and phenotypes of the other, forming feedback loops reminiscent of models of intraspecific social evolution. Here, we adapt the theory of...
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... date, most explorations of IIGEs have been studies providing empirical support for their likely existence and their contribution to trait variation. Examples of interspecific phenotypic manipulation are common in nature (Table 1), and many of these cases can be argued to be putative cases of IIGEs. One possible example occurs in arbuscular mycorrhizae, where the genotypes of fungal mutualists can alter root traits in the plants they inhabit (Gianinazzi-Pearson et al. 2007). ...Context 2
... or at least the potential for a prevalence of such effects, appear to be commonplace in many biological systems. In Table 1, we provide a breakdown of types of biological interaction in which there is a large literature suggesting importance of IIGE-like phenomena. These types of effects on trait expression across species, widely appreciated in their own specific contexts (Weis and Abrahamson 1986;Peacor and Werner 2001;Werner and Peacor 2003;Chen 2008;Thomas et al. 2012;O'Brien et al. 2021), have taken on a variety of different forms. ...Similar publications
Predicting evolution remains challenging. The field of quantitative genetics provides predictions for the response to directional selection through the breeder's equation, but these predictions can have errors. The sources of these errors include omission of traits under selection, inaccurate estimates of genetic variance, and nonlinearities in the...
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... (Estimated marginal means and corresponding 95% confidence limits.) of each other. Second, because niche construction in dung beetles is tightly linked to a maternally inherited microbiome, plasticity in niche construction and developmental responses to constructed environments inevitably create opportunities for non-genetic inheritance and indirect genetic effects (Baud et al., 2021;De Lisle et al., 2022) and for contributions to evolutionarily meaningful heritable variation residing outside the beetle genome. Here, much work remains to be done: for instance, we are only beginning to understand the degree of fidelity by which microbes are passaged throughout the Onthophagus life cycle and across Onthophagus generations. ...
Developmental plasticity is an important product of evolutionary processes, allowing organisms to maintain high fitness in the face of environmental perturbations. Once evolved, plasticity also has the potential to influence subsequent evolutionary outcomes, for example, by shaping phenotypic variation visible to selection and facilitating the emergence of novel trait variants. Furthermore, organisms may not just respond to environmental conditions through plasticity but may also actively modify the abiotic and (sym)biotic environments to which they themselves respond, causing plasticity to interact in complex ways with niche construction. Here, we explore developmental mechanisms and evolutionary consequences of plasticity in horned dung beetles. First, we discuss how post-invasion evolution of plasticity in an introduced Onthophagus species facilitated rapid range expansion and concurrent local adaptation of life history and morphology to novel climatic conditions. Second, we discuss how, in addition to plastically responding to variation in nutritional conditions, dung beetles engage in behaviors that modify the environment that they themselves respond to during later development. We document that these environment-modifying behaviors mask heritable variation for life history traits within populations, thereby shielding genetic variants from selection. Such cryptic genetic variation may be released and become selectable when these behaviors are compromised. Together, this work documents the complex interactions between plasticity, symbionts and niche construction, and highlights the usefulness of an integrative Eco–Evo–Devo framework to study the varied mechanisms and consequences of plasticity in development and evolution.
... Surprisingly, some populations of stickleback forego this immune response, letting the parasite grow relatively unchecked (De Lisle et al., 2022;Weber et al., 2022). Many of these populations upregulate fibrosis-suppression genes, indicating that they are actively suppressing this immune response (Lohman et al., 2017;Fuess et al., 2021). ...
... Furthermore, there is evidence of positive selection favoring fixation of large deletions within pro-fibrotic genes (Weber et al., 2022). This immune suppression suggests that there is a cost to the peritoneal fibrosis itself that could sometimes outweigh the cost of the parasite (De Lisle et al., 2022). Although this is an ongoing area of research, we know that the deleterious effects of fibrosis include lowered foraging success (De Lisle and Bolnick, 2021) and a reduction of fertility in both males and females (De Lisle and Bolnick, 2021;Weber et al., 2022). ...
The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response to Schistocephalus solidus infection in freshwater threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. We quantify the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are incidental costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induce fibrosis in stickleback and then test their C-start escape performance. Additionally, we measure the severity of fibrosis, body stiffness, and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model reveals that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide reaching and unexpected fitness consequences.
... 1,2 Because these weapons are deployed against the weapons of conspecific rivals, an aspect of the social environment that is itself evolving, male competition can generate consistent and intense directional selection for elaborations to weapon form that improve contest outcome. [3][4][5][6] For many weapons, this means increases in length or overall weapon size. 2,[7][8][9][10][11] Longer weapons permit a male to touch, strike, grab, or flip an opponent before that rival can do the same. ...
... Additionally, natural populations with this immune response have a lower prevalence of the parasite (Hund et al. 2022;Weber et al. 2022). Surprisingly, some populations of stickleback forego this immune response, letting the parasite grow relatively unchecked (De Lisle et al. 2022;Weber et al. 2022). Many of these populations up-regulate fibrosissuppression genes, indicating that they are actively suppressing this immune response (Lohman et al. 2017;Fuess et al. 2021). ...
... Furthermore, there is evidence of positive selection favoring fixation of large deletions within pro-fibrotic genes (Weber et al. 2022). This immune suppression suggests that there is a cost to the peritoneal fibrosis itself that could sometimes outweigh the cost of the parasite (De Lisle et al. 2022). Although this is an ongoing area of research, we know that the deleterious effects of fibrosis include lowered foraging success (De Lisle and Bolnick 2021) and a reduction of fertility in both males and females (De Lisle and Bolnick 2021;Weber et al. 2022). ...
The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response in threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. When freshwater stickleback are infected with the tapeworm parasite Schistocephalus solidus, they face an array of fitness consequences ranging from impaired body condition and fertility to an increased risk of mortality. To fight the infection, some stickleback will initiate a fibrosis immune response in which they produce excess collagenous tissue in their coelom. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. Here we quantify the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are collateral costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induce fibrosis in stickleback and then test their C-start escape performance. Additionally, we measure the severity of fibrosis, body stiffness, and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model reveals that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide reaching and unexpected fitness consequences.
... We recognise that, to some extent, the conflict-or-cooperation model can be considered an indirect genetic effect model since, from this perspective, the phenotype of a parasite can be influenced by the phenotypes of its social partners (i.e., intraspecific parasites) or coexisting parasite species (i.e. interspecific parasites) leading to social or group selection (Moore et al., 1997;McGlothlin et al., 2010;De Lisle et al., 2021). Therefore, an indirect genetic effect would also lead to similar interpretations to those expected in systems affected by the conflict-or-cooperation model. ...
The effect of parasites on host behaviour is generally considered an example of the extended phenotype, implying that parasite genes alter host behaviour to benefit the parasite. While the extended phenotype is a valid perspective supported by empirical examples, this approach was proposed from an evolutionary perspective and it does not fully explain all processes that occur at ecological time scales. For instance, the roles of the ontogenetic environment, memory and learning in forming the host phenotype are not explicitly mentioned. Furthermore, the cumulative effect of diverse populations or communities of parasites on host phenotype cannot be attributed to a particular genotype, much less to a particular gene. Building on the idea that the behaviour of a host is the result of a complex process, which certainly goes beyond a specific parasite gene, we use Niche Construction Theory to describe certain systems that are not generally the main focus in the extended phenotype model. We introduce three niche construction models with corresponding empirical examples that capture the diversity and complexity of host-parasite interactions, providing predictions that simpler models cannot generate. We hope that this novel perspective will inspire further research on the topic, given the impact of ecological factors on both short-, and long-term effects of parasitism.
... In this particular example, the selective environment is thus two-dimensional, but in nature selection is most likely multidimensional. The selective environment can also be described for both con-and heterospecific phenotype frequencies and the various social interactions that can arise from such interactions, sometimes in combination with path analytical tools (cf. Figure 4; see De Lisle et al., 2022;McGlothlin & Fisher, 2022;Wolf et al., 2001). This example illustrates the importance of measuring not only phenotypic traits and fitnesses, but also to quantify and (when possible) experimentally manipulate the local selective environments to gain a full understanding of selection. ...
In 1983, Russell Lande and Stevan Arnold published "The measurement of selection on correlated characters" which became a highly influential citation classic in evolutionary biology. This paper stimulated a cottage industry of field studies of natural and sexual selection in nature and resulted in several large-scale meta-analyses, statistical developments and method papers. The statistical tools they suggested contributed to a breakdown of the traditional dichotomy between ecological and evolutionary time scales and stimulated later developments such as "eco-evolutionary dynamics". However, regression-based selection analyses also became criticized from philosophical, methodological and statistical viewpoints and stimulated some still ongoing debates about causality in evolutionary biology. Here I return to this landmark paper by Lande and Arnold, analyse the controversies and debates it gave rise to and discuss the past, present and future of selection analyses in natural populations. A remaining legacy of Lande and Arnold (1983) are that studies of selection and inheritance can fruitfully be decoupled and be studied separately, since selection acts on phenotypes regardless of their genetic basis, and hence selection and evolutionary responses to selection are distinct processes.
... The extensive pairwise and higher-order genotype-by-genotype epistasis observed here means that the benefit of any given allele can vary depending on the social context (i.e., the genetic composition of the population), and this context dependence means that populations may evolve divergently and in response to locality-specific selective forces (La Fortezza & Velicer, 2021). More generally, social evolution and coevolution are analogous processes (De Lisle et al., 2022), and we therefore expect the geographic mosaics observed in coevolutionary systems to emerge in response to social selection (Thompson, 1994(Thompson, , 2005. The expectation of geographic mosaics necessitates the study of multiple populations, and care should be taken in extrapolating from observations of a single population to general outcomes of cooperation and conflict in the species as a whole. ...
Collective phenotypes, which arise from the interactions among individuals, can be important for the evolution of higher levels of biological organization. However, how a group's composition determines its collective phenotype remains poorly understood. When starved, cells of the social amoeba Dictyostelium discoideum cooperate to build a multicellular fruiting body, and the morphology of the fruiting body is likely advantageous to the surviving spores. We assessed how the number of strains, as well as their genetic and geographic relationships to one another, impact the group's morphology and productivity. We find that some strains consistently enhance or detract from the productivity of their groups, regardless of the identity of the other group members. We also detect extensive pairwise and higher-order genotype interactions, which collectively have a large influence on the group phenotype. Whereas previous work in Dictyostelium has focused almost exclusively on whether spore production is equitable when strains cooperate to form multicellular fruiting bodies, our results suggest a previously unrecognized impact of chimeric co-development on the group phenotype. Our results demonstrate how interactions among members of a group influence collective phenotypes and how group phenotypes might in turn impact selection on the individual.
... This framework of social impact and responsiveness can also be extended to interspecific interactions, because social evolution also occurs in contexts where the phenotype of an individual from one species influences the fitness of an individual of another species (De Lisle et al., 2022). This is strikingly clear in predator-prey or host-parasite interactions, where the directionality of the social interaction is often most evident in terms of impact and responsiveness. ...
Social evolution and the dynamics of social interactions have previously been studied under the frameworks of quantitative genetics and behavioural ecology. In quantitative genetics, indirect genetic effects of social partners on the socially plastic phenotypes of focal individuals typically lack crucial detail already included in treatments of social plasticity in behavioural ecology. Specifically, whilst focal individuals (e.g. receivers) may show variation in their 'responsiveness' to the social environment, individual social partners (e.g. signallers) may have a differential 'impact' on focal phenotypes. Here we propose an integrative framework, that highlights the distinction between responsiveness versus impact in indirect genetic effects for a range of behavioural traits. We describe impact and responsiveness using a reaction norm approach and provide statistical models for the assessment of these effects of focal and social partner identity in different types of social interactions. By providing such a framework, we hope to stimulate future quantitative research investigating the causes and consequences of social interactions on phenotypic evolution.
... Moore et al. [10] and others (e.g. [27]) introduce IGEs by further partitioning the environmental component, e, into a random, non-heritable component, e g , and a component, e z , that is affected by the trait value of another individual: z ¼ a þ e g þ e z : ...
... The 'social partners' (of past generations) need not coexist with the current population members to exert an effect on present trait value or selection in the present generation. Here, we will assume that ecological ancestors are conspecifics but this could be extended to explore the role of NC in coevolution in the same way that IGE theory has been expanded to heterospecifics [27]. ...
A central tenet of niche construction (NC) theory is that organisms can alter their environments in heritable and evolutionarily important ways, often altering selection pressures. We suggest that the physical changes niche constructors make to their environments may also alter trait heritability and the response of phenotypes to selection. This effect might change evolution, over and above the effect of NC acting via selection alone. We develop models of trait evolution that allow us to partition the effects of NC on trait heritability from those on selection to better investigate their distinct effects. We show that the response of a phenotype to selection and so the pace of phenotypic change can be considerably altered in the presence of NC and that this effect is compounded when trans-generational interactions are included. We argue that novel mathematical approaches are needed to describe the simultaneous effects of NC on trait evolution via selection and heritability. Just as indirect genetic effects have been shown to significantly increase trait heritability, the effects of NC on heritability in our model suggest a need for further theoretical development of the concept of heritability.
Mutualisms exhibit extensive context-dependent genetic variation in fitness outcomes. However, the specific traits that underpin fitness variation in mutualisms remain understudied. Pinpointing fitness-associated traits in mutualisms is critical to understanding how mutualisms evolve, as well as identifying the mechanisms that maintain genetic variation for fitness in interacting populations. In this study, we quantified the contribution of host and symbiont genotypes to variation in resource exchange, use, and production traits measured in the host using the model mutualism between legumes and nitrogen fixing rhizobia as our study system. We predicted that plant genotype x rhizobia genotype (GxG) effects would be common to resource exchange traits because resource exchange is hypothesized to be governed by input from both interacting partners through bargaining. On the other hand, we predicted that plant genotype effects would be common to host resource use and production traits because these traits are indirectly related to the exchange of resources. Consistent with our prediction for resource exchange traits, but not our prediction for resource use and production traits, we found that rhizobia genotype and GxG effects were the most common sources of variation in the traits that we measured. The results of this study complement the commonly observed phenomenon of GxG effects for fitness by showing that numerous mutualism traits also exhibit GxG variation. Furthermore, they highlight the possibility that the exchange of resources as well as how partners use and produce traded resources can influence the evolution of mutualistic interactions. Future studies can now quantify the relationship between resource exchange, use and production traits and fitness (i.e. selection) to test the competing hypotheses proposed to explain the maintenance of fitness variation in mutualisms.
