Holobiont Evolution: Mathematical Model with Vertical vs. Horizontal Microbiome Transmission

A holobiont is a composite organism consisting of a host together with its microbiome, such as a coral with its zooxanthellae. To explain the often intimate integration between hosts and their microbiomes, some investigators contend that selection operates on holobionts as a unit and view the microbiome’s genes as extending the host’s nuclear genome to jointly comprise a hologenome. Because vertical transmission of microbiomes is uncommon, other investigators contend that holobiont selection cannot be effective because a holobiont’s microbiome is an acquired condition rather than an inherited trait. This disagreement invites a simple mathematical model to see how holobiont selection might operate and to assess its plausibility as an evolutionary force. This paper presents two variants of such a model. In one variant, juvenile hosts obtain microbiomes from their parents (vertical transmission). In the other variant, microbiomes of juvenile hosts are assembled from source pools containing the combined microbiomes of all parents (horizontal transmission). According to both variants, holobiont selection indeed causes evolutionary change in holobiont traits. Therefore, holobiont selection is plausibly an effective evolutionary force with either mode of microbiome transmission. The modeling employs two distinct concepts of inheritance, depending on the mode of microbiome transmission: collective inheritance whereby juveniles inherit a sample of the collected genomes from all parents, as contrasted with lineal inheritance whereby juveniles inherit the genomes from only their own parents. A distinction between collective and lineal inheritance also features in theories of multilevel selection

Extra-Pair Paternity in Birds: Review of the Genetic Benefits

Question: How well are genetic benefits hypotheses for extra-pair paternity supported by empirical evidence? Data incorporated: Almost all published studies testing for genetic benefits from 1980 onwards (121 papers, 55 species). Analysis methods: Collected key features and findings of each study in a database. Determined overall level of support for both good genes and compatible genes hypotheses. Conducted a formal meta-analysis on a subset of studies asking the following questions: (1) Do extra-pair mates of females have different phenotypes than their within-pair mates? (2) Do extra-pair offspring differ in viability from within-pair offspring? (3) Is there a correlation between the genetic similarity of a social pair and the incidence of extra-pair paternity? Results: Both the good genes and compatible genes hypotheses failed to be supported in more than half of the species studied. The meta-analysis shows that extra-pair males are on average larger and older than within-pair males, but not different in terms of secondary sexual traits, condition or relatedness to the female. No difference was found between extra-pair and within-pair young in survival to the next breeding season. We found no significant correlation between pair genetic similarity and extra-pair paternity. Conclusions: Genetic benefits are not strongly supported by available empirical data. New hypotheses are needed

Extra-Pair Parentage: A New Theory Based on Transactions in a Cooperative Game

Question: What is the adaptive significance of extra-pair parentage? Theoretical approach:We view parentage as a ‘transaction currency’ for exchanges of ecological benefits. We develop a multi-player cooperative game, using the core and the Nash bargaining solution as solution concepts. Model assumptions: Birds can negotiate about who pairs with whom. Parentage can be exchanged between individuals as a result of negotiations. Number of offspring fledged from a nest depends on the experience and situation of the social parents and not on their genes (i.e. only direct benefits, no genetic benefits). Predictions: We predict extra-pair parentage to occur when individuals with higher breeding capability are paired to individuals with lower breeding capability. Social interactions between males are predicted to precede the occurrence of extra-pair paternity. We give an example experiment to test our model

The Evolution of Payoff Matrices: Providing Incentives to Cooperate

Most of the work in evolutionary game theory starts with a model of a social situation that gives rise to a particular payoff matrix and analyses how behaviour evolves through natural selection. Here, we invert this approach and ask, given a model of how individuals behave, how the payoff matrix will evolve through natural selection. In particular, we ask whether a prisoner’s dilemma game is stable against invasions by mutant genotypes that alter the payoffs. To answer this question, we develop a two-tiered framework with goal-oriented dynamics at the behavioural time scale and a diploid population genetic model at the evolutionary time scale. Our results are two-fold: first, we show that the prisoner’s dilemma is subject to invasions by mutants that provide incentives for cooperation to their partners, and that the resulting game is a coordination game similar to the hawk – dove game. Second, we find that for a large class of mutants and symmetric games, a stable genetic polymorphism will exist in the locus determining the payoff matrix, resulting in a complex pattern of behavioural diversity in the population. Our results highlight the importance of considering the evolution of payoff matrices to understand the evolution of animal social systems

Biological Institutions: The Political Science of Animal Cooperation

Social evolution is one of the most rapidly developing areas in evolutionary biology. A main theme is the emergence of cooperation among organisms, including the factors that impede cooperation. Although animal societies seem to have no formal institutions, such as courts or legislatures, we argue that biology presents many examples where an interaction can properly be thought of as an informal institution, meaning there are evolved norms and structure to the interaction that enable parties to reach mutually beneficial outcomes. These informal institutions are embedded in the natural history of the interaction, in factors such as where and when parties interact, how long and how close they stay together, and so on. Institutional theory thus widens the scope of behavioral ecology by considering not only why animals evolve to choose the strategies they choose, but also asking both why it is that they find themselves in those particular interaction setups and how these particular interactions can be sustained. Institutions frequently enable interacting parties avoid inefficient outcomes and support efficient exchange among agents with conflicting interests. The main thesis of this paper is that the organization of many biological interactions can properly be understood as institutions that enable mutually beneficial outcomes to be achieved relative to an unstructured interaction. To do this, institutions resolve or regulate the conflicts of interests among parties. The way conflicts of interests affect the outcome depends on the structure of the interaction, which can create problems of commitment, coordination and private information. Institutional theory focuses on how to address each of these issues, typically focusing on the development of social norms, rules, and other constraints on individual behaviors. We illustrate our thesis with examples from cooperative breed and genes as within-body-mechanism-design

The Perfect Family: Decision Making in Biparental Care

Background Previous theoretical work on parental decisions in biparental care has emphasized the role of the conflict between evolutionary interests of parents in these decisions. A prominent prediction from this work is that parents should compensate for decreases in each other\u27s effort, but only partially so. However, experimental tests that manipulate parents and measure their responses fail to confirm this prediction. At the same time, the process of parental decision making has remained unexplored theoretically. We develop a model to address the discrepancy between experiments and the theoretical prediction, and explore how assuming different decision making processes changes the prediction from the theory. Model Description We assume that parents make decisions in behavioral time. They have a fixed time budget, and allocate it between two parental tasks: provisioning the offspring and defending the nest. The proximate determinant of the allocation decisions are parents\u27 behavioral objectives. We assume both parents aim to maximize the offspring production from the nest. Experimental manipulations change the shape of the nest production function. We consider two different scenarios for how parents make decisions: one where parents communicate with each other and act together (the perfect family), and one where they do not communicate, and act independently (the almost perfect family). Conclusions/Significance The perfect family model is able to generate all the types of responses seen in experimental studies. The kind of response predicted depends on the nest production function, i.e. how parents\u27 allocations affect offspring production, and the type of experimental manipulation. In particular, we find that complementarity of parents\u27 allocations promotes matching responses. In contrast, the relative responses do not depend on the type of manipulation in the almost perfect family model. These results highlight the importance of the interaction between nest production function and how parents make decisions, factors that have largely been overlooked in previous models

Evolution's rainbow: diversity, gender, and sexuality in nature and people

In this innovative celebration of diversity and affirmation of individuality in animals and humans, Joan Roughgarden challenges accepted wisdom about gender identity and sexual orientation. A distinguished evolutionary biologist, Roughgarden takes on the medical establishment, the Bible, social science - and even Darwin himself. She leads the reader through a fascinating discussion of diversity in gender and sexuality among fish, reptiles, amphibians, birds, and mammals, including primates. Evolution's Rainbow explains how this diversity develops from the action of genes and hormones and how people come to differ from each other in all aspects of body and behavior. Roughgarden reconstructs primary science in light of feminist, gay, and transgender criticism and redefines our understanding of sex, gender, and sexuality. Witty, playful, and daring, this book will revolutionize our understanding of sexuality. Roughgarden argues that principal elements of Darwinian sexual selection theory are false and suggests a new theory that emphasizes social inclusion and control of access to resources and mating opportunity. She disputes a range of scientific and medical concepts, including Wilson's genetic determinism of behavior, evolutionary psychology, the existence of a gay gene, the role of parenting in determining gender identity, and Dawkins's "selfish gene" as the driver of natural selection. She dares social science to respect the agency and rationality of diverse people; shows that many cultures across the world and throughout history accommodate people we label today as lesbian, gay, and transgendered; and calls on the Christian religion to acknowledge the Bible's many passages endorsing diversity in gender and sexuality. Evolution's Rainbow concludes with bold recommendations for improving education in biology, psychology, and medicine; for democratizing genetic engineering and medical practice; and for building a public monument to affirm diversity as one of our nation's defining principles