The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes

The question of how genetic variation translates into organismal diversity has puzzled biologists for decades. Despite recent advances in evolutionary and developmental genetics, the mechanisms that underlie adaptation, diversification and evolutionary innovation remain largely unknown. The exceptionally diverse species flocks of cichlid fishes are textbook examples of adaptive radiation and explosive speciation and emerge as powerful model systems to study the genetic basis of animal diversification. East Africa's hundreds of endemic cichlid species are akin to a natural mutagenesis screen and differ greatly not only in ecologically relevant (hence naturally selected) characters such as mouth morphology and body shape, but also in sexually selected traits such as coloration. One of the most fascinating aspects of cichlid evolution is the frequent occurrence of evolutionary parallelisms, which has led to the question whether selection alone is sufficient to produce these parallel morphologies, or whether a developmental or genetic bias has influenced the direction of diversification. Here, I review fitness-relevant traits that could be responsible for the cichlids' evolutionary success and assess whether these were shaped by sexual or natural selection. I then focus on the interaction and the relative importance of sexual vs. natural selection in cichlid evolution. Finally, I discuss what is currently known about the genes underlying the morphogenesis of adaptively relevant traits and highlight the importance of the forthcoming cichlid genomes in the quest of the genetic basis of diversification in this group.     

A critique of Darwinian anthropology

Darwinian anthropology holds that human behavior is adaptive in the sense of being designed to maximize reproductive success and that measurement of reproductive differentials typically illuminates adaptation. I argue to the contrary, that adaptive design is usually manifested at the psychological rather than at the behavioral level, that measuring reproductive differentials is at best an inefficient and ambiguous way to illuminate adaptation, and that Darwin's theory of natural selection sheds light on human affairs only insofar as it promotes understanding of the psychology that underpins these affairs.     

The emotion system promotes diversity and evolvability

Studies on the relationship between the optimal phenotype and its environment have had limited focus on genotype-to-phenotype pathways and their evolutionary consequences. Here, we study how multi-layered trait architecture and its associated constraints prescribe diversity. Using an idealized model of the emotion system in fish, we find that trait architecture yields genetic and phenotypic diversity even in absence of frequency-dependent selection or environmental variation. That is, for a given environment, phenotype frequency distributions are predictable while gene pools are not. The conservation of phenotypic traits among these genetically different populations is due to the multi-layered trait architecture, in which one adaptation at a higher architectural level can be achieved by several different adaptations at a lower level. Our results emphasize the role of convergent evolution and the organismal level of selection. While trait architecture makes individuals more constrained than what has been assumed in optimization theory, the resulting populations are genetically more diverse and adaptable. The emotion system in animals may thus have evolved by natural selection because it simultaneously enhances three important functions, the behavioural robustness of individuals, the evolvability of gene pools and the rate of evolutionary innovation at several architectural levels.     

THE NICHE CONSTRUCTION PERSPECTIVE: A CRITICAL APPRAISAL

Niche construction refers to the activities of organisms that bring about changes in their environments, many of which are evolutionarily and ecologically consequential. Advocates of niche construction theory (NCT) believe that standard evolutionary theory fails to recognize the full importance of niche construction, and consequently propose a novel view of evolution, in which niche construction and its legacy over time (ecological inheritance) are described as evolutionary processes, equivalent in importance to natural selection. Here, we subject NCT to critical evaluation, in the form of a collaboration between one prominent advocate of NCT, and a team of skeptics. We discuss whether niche construction is an evolutionary process, whether NCT obscures or clarifies how natural selection leads to organismal adaptation, and whether niche construction and natural selection are of equivalent explanatory importance. We also consider whether the literature that promotes NCT overstates the significance of niche construction, whether it is internally coherent, and whether it accurately portrays standard evolutionary theory. Our disagreements reflect a wider dispute within evolutionary theory over whether the neo‐Darwinian synthesis is in need of reformulation, as well as different usages of some key terms (e.g., evolutionary process).     

Rupert Riedl and the re-synthesis of evolutionary and developmental biology: body plans and evolvability

This paper reviews the scientific career of Rupert Riedl and his contributions to evolutionary biology. Rupert Riedl, a native of Vienna, Austria, began his career as a marine biologist who made important contributions to the systematics and anatomy of major invertebrate groups, as well as to marine ecology. When he assumed a professorship at the University of North Carolina in 1968, the predominant thinking in evolutionary biology focused on population genetics, to the virtual exclusion of most of the rest of biology. In this atmosphere Riedl developed his "systems theory" of evolution, which emphasizes the role of functional and developmental integration in limiting and enabling adaptive evolution by natural selection. The main objective of this theory is to account for the observed patterns of morphological evolution, such as the conservation of body plans. In contrast to other "alternative" theories of evolution, Riedl never denied the importance of natural selection as the driving force of evolution, but thought it necessary to contextualize natural selection with the organismal boundary conditions of adaptation. In Riedl's view development is the most important factor besides natural selection in shaping the pattern and processes of morphological evolution.     

Kin selection under blending inheritance

Why did Darwin fail to develop his insights on kin selection into a proper theory of social adaptation? One suggestion has been that his inadequate understanding of heredity kept the problem out of focus. Here, I determine whether it is possible to develop a quantitative theory of kin selection upon the assumption of blending inheritance. I find that, whilst Hamilton's rule of kin selection can be readily derived under the assumption of blending inheritance, this mechanism complicates the computation of relatedness coefficients, and can even cause them to fluctuate over generations. Nevertheless, I show that the ultimate criterion for selection to favour any social trait - i.e. a time-average of Hamilton's rule - remains the same as under particulate inheritance. By eliminating the gene from the theory of kin selection, I clarify the role that it plays in the theory of social adaptation.     

Natural selection and the limitations of environmental resources

In this paper, I am clarifying and defending my argument (Nanay 2005) in favor of the claim that cumulative selection can explain adaptation provided that the environmental resources are limited. Further, elaborate on what this limitation of environmental resources means and why it is relevant for the explanatory power of natural selection.     

Convergent evolution and divergent selection: lizards at the White Sands ecotone

Ecological transition zones, where organismal phenotypes result from a delicate balance between selection and migration, highlight the interplay of local adaptation and gene flow. Here, I study the response of an entire species assemblage to natural selection across a common ecotone. Three lizard species, distributed along a dramatic environmental gradient in substrate color, display convergent adaptation of blanched coloration on the gypsum dunes of White Sands National Monument. I investigate the role of gene flow in modulating phenotypic response to selection by quantifying color variation and genetic variation across the ecotone. I find species differences in degree of background matching and in genetic connectivity of populations across the ecotone. Differences among species in phenotypic response to selection scale precisely to levels of genetic isolation. Species with higher levels of gene flow across the ecotone exhibit less dramatic responses to selection. Results also reveal a strong signal of ecologically mediated divergence for White Sands lizards. For all species, phenotypic variation is better explained by habitat similarity than genetic similarity. Convergent evolution of blanched coloration at White Sands clearly reflects the action of strong divergent selection; however, adaptive response appears to be modulated by gene flow and demographic history and can be predicted by divergence-with-gene-flow models.     

GENETIC CONSTRAINTS ON ADAPTATION TO A CHANGING ENVIRONMENT

Genetic correlations between traits can constrain responses to natural selection. To what extent such correlations limit adaptation depends on patterns of directional selection. I derive the expected rate of adaptation (or evolvability) under randomly changing selection gradients. When directional selection gradients have an arbitrary covariance matrix, the average rate of adaptation depends on genetic correlations between traits, contrary to the isotropic case investigated in previous studies. Adaptation may be faster on average with more genetic correlation between traits, if these traits are selected to change jointly more often than the average pair of traits. However, natural selection maximizes the long‐term fitness of a population, not necessarily its rate of adaptation. I therefore derive the average lag load caused by deviations of the mean phenotype from an optimum, under several forms of environmental changes typically experienced by natural populations, both stochastic and deterministic. Simple formulas are produced for how the G matrix affects long‐term fitness in these contexts, and I discuss how their parameters can be estimated empirically.     

Life,the universe and everything

The Formal Darwinism project probes the connections between the dynamics of natural selection and the design of organisms. Here, I explain why this work should be of interest to philosophers, arguing that it is the natural development in a long-running scholarly enquiry into the meaning of life. I then review some of my own work which has applied the tools of Formal Darwinism to address issues concerning the units of adaptation in social evolution, leading to a deeper understanding of the adaptation of individual organisms. Finally, I sketch some directions Formal Darwinism to explore beyond the biological sciences, with a focus upon cosmology.     

Adaptation as process: the future of Darwinism and the legacy of Theodosius Dobzhansky

Conceptions of adaptation have varied in the history of genetic Darwinism depending on whether what is taken to be focal is the process of adaptation, adapted states of populations, or discrete adaptations in individual organisms. I argue that Theodosius Dobzhansky's view of adaptation as a dynamical process contrasts with so-called "adaptationist" views of natural selection figured as "design-without-a-designer" of relatively discrete, enumerable adaptations. Correlated with these respectively process and product oriented approaches to adaptive natural selection are divergent pictures of organisms themselves as developmental wholes or as "bundles" of adaptations. While even process versions of genetical Darwinism are insufficiently sensitive to the fact much of the variation on which adaptive selection works consists of changes in the timing, rate, or location of ontogenetic events, I argue that articulations of the Modern Synthesis influenced by Dobzhansky are more easily reconciled with the recent shift to evolutionary developmentalism than are versions that make discrete adaptations central.     

Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.     

Evolutionary games under incompetence

The adaptation process of a species to a new environment is a significant area of study in biology. As part of natural selection, adaptation is a mutation process which improves survival skills and reproductive functions of species. Here, we investigate this process by combining the idea of incompetence with evolutionary game theory. In the sense of evolution, incompetence and training can be interpreted as a special learning process. With focus on the social side of the problem, we analyze the influence of incompetence on behavior of species. We introduce an incompetence parameter into a learning function in a single-population game and analyze its effect on the outcome of the replicator dynamics. Incompetence can change the outcome of the game and its dynamics, indicating its significance within what are inherently imperfect natural systems.

     

The practice of classification and the theory of evolution,and what the demise of Charles Darwin's tree of life hypothesis means for both of them

Debates over the status of the tree of life (TOL) often proceed without agreement as to what it is supposed to be: a hierarchical classification scheme, a tracing of genomic and organismal history or a hypothesis about evolutionary processes and the patterns they can generate. I will argue that for Darwin it was a hypothesis, which lateral gene transfer in prokaryotes now shows to be false. I will propose a more general and relaxed evolutionary theory and point out why anti-evolutionists should take no comfort from disproof of the TOL hypothesis.     

The Difference Between Selection and Drift: A Reply to Millstein

Millstein [Bio. Philos. 17 (2002) 33] correctly identies a serious problem with the view that natural selection and random drift are not conceptually distinct. She offers a solution to this problem purely in terms of differences between the processes of selection and drift. I show that this solution does not work, that it leaves the vast majority of real biological cases uncategorized. However, I do think there is a solution to the problem she raises, and I offer it here. My solution depends on solving the biological analogue of the reference class problem in probability theory and on the reality of individual fitnesses.     

Extended Phenotypes and Extended Organisms

Phenotype, whether conventional or extended, is defined as a reflectionof an underlying genotype. Adaptation and the natural selection thatfollows from it depends upon a progressively harmonious fit betweenphenotype and environment. There is in Richard Dawkins' notion ofthe extended phenotype a paradox that seems to undercut conventionalviews of adaptation, natural selection and adaptation. In a nutshell, ifthe phenotype includes an organism's environment, how then can theorganism adapt to itself? The paradox is resolvable through aphysiological, as opposed to a genetic, theory of natural selection andadaptation.     

Levels of selection and the formal Darwinism project

Understanding good design requires addressing the question of what units undergo natural selection, thereby becoming adapted. There is, therefore, a natural connection between the formal Darwinism project (which aims to connect population genetics with the evolution of design and fitness maximization) and levels of selection issues. We argue that the formal Darwinism project offers contradictory and confusing lines of thinking concerning level(s) of selection. The project favors multicellular organisms over both the lower (cell) and higher (social group) levels as the level of adaptation. Grafen offers four reasons for giving such special status to multicellular organisms: (1) they lack appreciable within-organism cell selection, (2) they have multiple features that appear contrived for the same purpose, (3) they possess a set of phenotypes, and (4) they leave offspring according to their phenotypes. We discuss why these rationales are not compelling and suggest that a more even-handed approach, in which multicellular organisms are not assumed to have special status, would be desirable for a project that aims to make progress on the foundations of evolutionary theory.     

The distribution of fitness effects among beneficial mutations

We know little about the distribution of fitness effects among new beneficial mutations, a problem that partly reflects the rarity of these changes. Surprisingly, though, population genetic theory allows us to predict what this distribution should look like under fairly general assumptions. Using extreme value theory, I derive this distribution and show that it has two unexpected properties. First, the distribution of beneficial fitness effects at a gene is exponential. Second, the distribution of beneficial effects at a gene has the same mean regardless of the fitness of the present wild-type allele. Adaptation from new mutations is thus characterized by a kind of invariance: natural selection chooses from the same spectrum of beneficial effects at a locus independent of the fitness rank of the present wild type. I show that these findings are reasonably robust to deviations from several assumptions. I further show that one can back calculate the mean size of new beneficial mutations from the observed mean size of fixed beneficial mutations.     

The population genetics of adaptation: the adaptation of DNA sequences

I describe several patterns characterizing the genetics of adaptation at the DNA level. Following Gillespie (1983, 1984, 1991), I consider a population presently fixed for the ith best allele at a locus and study the sequential substitution of favorable mutations that results in fixation of the fittest DNA sequence locally available. Given a wild type sequence that is less than optimal, I derive the fitness rank of the next allele typically fixed by natural selection as well as the mean and variance of the jump in fitness that results when natural selection drives a substitution. Looking over the whole series of substitutions required to reach the best allele, I show that the mean fitness jumps occurring throughout an adaptive walk are constrained to a twofold window of values, assuming only that adaptation begins from a reasonably fit allele. I also show that the first substitution and the substitution of largest effect account for a large share of the total fitness increase during adaptation. I further show that the distribution of selection coefficients fixed throughout such an adaptive walk is exponential (ignoring mutations of small effect), a finding reminiscent of that seen in Fisher's geometric model of adaptation. Last, I show that adaptation by natural selection behaves in several respects as the average of two idealized forms of adaptation, perfect and random.     

Evolutionary Developmental Biology and Human Language Evolution: Constraints on Adaptation

A tension has long existed between those biologists who emphasize the importance of adaptation by natural selection and those who highlight the role of phylogenetic and developmental constraints on organismal form and function. This contrast has been particularly noticeable in recent debates concerning the evolution of human language. Darwin himself acknowledged the existence and importance of both of these, and a long line of biologists have followed him in seeing, in the concept of ??descent with modification??, a framework naturally able to incorporate both adaptation and constraint. Today, the integrated perspective of modern evolutionary developmental biology (??evo-devo??) allows a more subtle and pluralistic approach to these traditional questions, and has provided several examples where the traditional notion of ??constraint?? can be cashed out in specific, mechanistic terms. This integrated viewpoint is particularly relevant to the evolution of the multiple mechanisms underlying human language, because of the short time available for novel aspects of these mechanisms to evolve and be optimized. Comparative data indicate that many cognitive aspects of human language predate humans, suggesting that pre-adaptation and exaptation have played important roles in language evolution. Thus, substantial components of what many linguists call ??Universal Grammar?? predate language itself. However, at least some of these older mechanisms have been combined in ways that generate true novelty. I suggest that we can insightfully exploit major steps forward in our understanding of evolution and development, to gain a richer understanding of the principles that underlie human language evolution.