Biology subjects

McGlothlin, J. W.

Publications and source records attributed to McGlothlin, J. W..

7 recordsLinked to original sources

bioRxiv2026

Pick your poison: Tetrodotoxin variants give Pacific newts a potential leg up in the coevolutionary arms race with resistant garter snake predators

Coevolution proceeds through the evolution of traits that mediate ecological interactions and evolutionary outcomes. In the arms race between toxic Pacific newts (Taricha) and their garter snake predators (Thamnophis), this interface involves tetrodotoxin (TTX), an antipredator defense that inhibits nerve and muscle function by blocking voltage-gated sodium channels. In response, snakes have evolved TTX-resistant channels, in some cases leading to snake populations that are nearly invulnerable to TTX. For decades, newt TTX has been treated as a single defensive trait, yet TTX occurs as a family of structurally related analogs that may represent alternative defenses against snakes. Here, we characterize TTX analog diversity in all four species of Taricha and evaluate how these compounds interact with sodium channels in coevolved garter snakes. Using LC-MS analysis of newt skin secretions, we detected a diverse suite of TTX analogs previously unrecognized in Pacific newts. We then used molecular docking models to evaluate interactions between various TTX analogs and variants of the skeletal muscle channel (NaV1.4) that span the range of TTX resistance in garter snakes. We found that some TTX analogs docked better than canonical TTX in resistant snake channels. Notably, we show that 11-deoxy-4-epi-TTX and 11-deoxy-TTX have favorable interactions with hydrophobic amino-acid substitutions in extremely resistant garter snake sodium channels, potentially circumventing predator resistance to canonical TTX. Our results suggest a complex arms race involving multiple newt TTX analogs and multiple snake sodium channel variants. As such, newts may keep pace with snakes by diversifying their arsenal of chemical weapons. SignificanceIn western North America, some newts have enough toxin in their skin to kill most predators, but coevolution has led to toxin resistance in their garter snake predators that in some cases is so extreme that snakes should be able to withstand more toxin than newts could possibly possess. Here, we explore the possibility that newts may be able to fight back against these resistant predators through the by evolving a diverse repertoire of toxins. We use chemical analyses and computational modeling to show that newts have a wide variety of toxins, some of which are likely to be more effective against resistant snakes, suggesting that coevolution may continue to occur even when snakes become very resistant.

evolutionary biology↗

bioRxiv2021

Runaway evolution from male-male competition

Wondrously elaborate weapons and displays that appear to be counter to ecological optima are widespread features of male contests for mates across the animal kingdom. To understand how such diverse traits evolve, here we develop a quantitative genetic model of sexual selection for a male signaling trait that mediates aggression in male-male contests and show that an honest indicator of aggression can generate selection on itself by altering the social environment. This can cause selection to accelerate as the trait is elaborated, leading to runaway evolution. Thus, an evolving source of selection provided by the social environment is the fundamental unifying feature of runaway sexual selection driven by either male-male competition or female mate choice. However, a key difference is that runaway driven by male-male competition requires signal honesty. Our model identifies simple conditions that provide clear, testable predictions for empirical studies using standard quantitative genetic methods.

evolutionary biology↗

bioRxiv2021

Interacting Phenotypes and the Coevolutionary Process

Coevolution occurs when species interact to influence one anothers 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 within-species social evolution, characterized by indirect genetic effects and social selection imposed by interacting individuals, to the case of interspecific interactions. In a trait-based model, we derive general expressions for multivariate evolutionary change in two species and the expected between-species covariance in evolutionary change when selection varies across space. We show that reciprocal interspecific indirect genetic effects can dominate the coevolutionary process and drive patterns of correlated evolution beyond what is expected from direct selection alone. In extreme cases, interspecific indirect genetic effects can lead to coevolution when selection does not covary between species or even when one species lacks genetic variance. Moreover, our model indicates that interspecific indirect genetic effects may interact in complex ways with cross-species selection to determine the course of coevolution. Importantly, our model makes empirically testable predictions for how different forms of reciprocal interactions contribute to the coevolutionary process.

evolutionary biology↗

bioRxiv2021

A Synthesis of Game Theory and Quantitative Genetic Models of Social Evolution

Two popular approaches for modeling social evolution, evolutionary game theory and quantitative genetics, ask complementary questions but are rarely integrated. Game theory focuses on evolutionary outcomes, with models solving for evolutionarily stable equilibria, whereas quantitative genetics provides insight into evolutionary processes, with models predicting short-term responses to selection. Here we draw parallels between evolutionary game theory and interacting phenotypes theory, which is a quantitative genetic framework for understanding social evolution. First, we show how any evolutionary game may be translated into two quantitative genetic selection gradients, nonsocial and social selection, which may be used to predict evolutionary change from a single round of the game. We show that synergistic fitness effects may alter predicted selection gradients, causing changes in magnitude and sign as the population mean evolves. Second, we show how evolutionary games involving plastic behavioral responses to partners can be modeled using indirect genetic effects, which describe how trait expression changes in response to genes in the social environment. We demonstrate that repeated social interactions in models of reciprocity generate indirect effects and conversely, that estimates of parameters from indirect genetic effect models may be used to predict the evolution of reciprocity. We argue that a pluralistic view incorporating both theoretical approaches will benefit empiricists and theorists studying social evolution. We advocate the measurement of social selection and indirect genetic effects in natural populations to test the predictions from game theory, and in turn, the use of game theory models to aid in the interpretation of quantitative genetic estimates.

evolutionary biology↗

bioRxiv2021

Gene conversion facilitates the adaptive evolution of self-resistance in highly toxic newts

Reconstructing the histories of complex adaptations and identifying the evolutionary mechanisms underlying their origins are two of the primary goals of evolutionary biology. Taricha newts, which contain high concentrations of the deadly toxin tetrodotoxin (TTX) as an antipredator defense, have evolved resistance to self-intoxication, which is a complex adaptation requiring changes in six paralogs of the voltage-gated sodium channel (Nav) gene family, the physiological target of TTX. Here, we reconstruct the origins of TTX self-resistance by sequencing the entire Nav gene family in newts and related salamanders. We show that moderate TTX resistance evolved early in the salamander lineage in three of the six Nav paralogs, preceding the proposed appearance of tetrodotoxic newts by [~]100 million years. TTX-bearing newts possess additional unique substitutions across the entire Nav gene family that provide physiological TTX resistance. These substitutions coincide with signatures of positive selection and relaxed purifying selection, as well as gene conversion events, that together likely facilitated their evolution. We also identify a novel exon duplication within Nav1.4 encoding an expressed TTX-binding site. Two resistance-conferring changes within newts appear to have spread via nonallelic gene conversion: in one case, one codon was copied between paralogs, and in the second, multiple substitutions were homogenized between the duplicate exons of Nav1.4. Our results demonstrate that gene conversion can accelerate the coordinated evolution of gene families in response to a common selection pressure.

evolutionary biology↗

bioRxiv2021

Social selection and the evolution of maladaptation

Evolution by natural selection is often viewed as a process that inevitably leads to adaptation, or an increase in population fitness over time. However, maladaptation, an evolved decrease in fitness, may also occur in response to natural selection under some conditions. Social selection, which arises from the effects of social partners on fitness, has been identified as a potential cause of maladaptation, but we lack a general rule identifying when social selection should lead to a decrease in population mean fitness. Here we use a quantitative genetic model to develop such a rule. We show that maladaptation is most likely to occur when social selection is strong relative to nonsocial selection and acts in an opposing direction. In this scenario, the evolution of traits that impose fitness costs on others may outweigh evolved gains in fitness for the individual, leading to a net decrease in population mean fitness. Further, we find that maladaptation may also sometimes occur when phenotypes of interacting individuals negatively covary. We outline the biological situations where maladaptation in response to social selection can be expected, provide both quantitative genetic and phenotypic versions of our derived result, and suggest what empirical work would be needed to test it. We also consider the effect of social selection on inclusive fitness and support previous work showing that inclusive fitness cannot suffer an evolutionary decrease. Taken together, our results show that social selection may decrease population mean fitness when it opposes individual-level selection, even as inclusive fitness increases. Subject areaQuantitative genetics and Mendelian inheritance

evolutionary biology↗

bioRxiv2021

Conservation and convergence of genetic architecture in the adaptive radiation of Anolis lizards

The G matrix, which quantifies the genetic architecture of traits, is often viewed as an evolutionary constraint. However, G can evolve in response to selection and may also be viewed as a product of adaptive evolution. Convergent evolution of G in similar environments would suggest that G evolves adaptively, but it is difficult to disentangle such effects from phylogeny. Here, we use the adaptive radiation of Anolis lizards to ask whether convergence of G accompanies the repeated evolution of habitat specialists, or ecomorphs, across the Greater Antilles. We measured G in seven species representing three ecomorphs (trunk-crown, trunk- ground, and grass-bush). We found that the overall structure of G does not converge. Instead, the structure of G is well conserved and displays a phylogenetic signal consistent with Brownian motion. However, several elements of G showed signatures of convergence, indicating that some aspects of genetic architecture have been shaped by selection. Most notably, genetic correlations between limb traits and body traits were weaker in long-legged trunk-ground species, suggesting effects of recurrent selection on limb length. Our results demonstrate that common selection pressures may have subtle but consistent effects on the evolution of G, even as its overall structure remains conserved.

evolutionary biology↗