Phylogenetic tests of the sensory exploitation model of sexual selection

The diverse characteristics among closely related species are often involved in communication between the sexes. The traditional view that intersexual communication behaviors evolve in a complementary way is called into question by the sensory exploitation hypothesis. By predicting a lack of coordinated evolution between signals and preferences, the sensory exploitation hypothesis is distinct from other mechanisms of sexual selection. Tests of sensory exploitation have taken a multi-disciplinary approach, with insights from sensory physiology, behavior and phylogenetic comparisons. By demonstrating that signals and receivers are not closely coupled, and that signal preference pre-dates signal origin, proponents of the model argue that sensory exploitation is an evolutionary force responsible for the diversification of intersexual communication signals.     

Genetic explorations of recent human metabolic adaptations: hypotheses and evidence

Since humans and chimpanzees split from a common ancestor over 6 million years ago, human metabolism has changed dramatically. This change includes adaptations to a high-quality diet, the evolution of an energetically expensive brain, dramatic increases in endurance abilities, and capacity for energy storage in white adipose tissue. Human metabolism continues to evolve in modern human populations in response to local environmental and cultural selective forces. Understanding the nature of these selective forces and the physiological responses during human evolution is a compelling challenge for evolutionary biologists. The complex genetic architecture surrounding metabolic phenotypes indicates that selection probably altered allelic frequencies across many loci in populations experiencing adaptive metabolic change to fit their environment. A recent analysis supports this hypothesis, finding that classic selective sweeps at single loci were rare during the past 250 000 years of human evolution. Detection of selective signatures at multiple loci, as well as exploration of physiological adaptation to environment in humans, will require cross-disciplinary collaboration, including the incorporation of biological pathway analysis. This review explores the Thrifty Genotype Hypothesis, high-altitude adaptation, cold-resistance adaptation, and genetic evidence surrounding these proposed metabolic adaptations in an attempt to clarify current challenges and avenues for future progress.     

Sensory bias as an explanation for the evolution of mate preferences

The sensory bias model of sexual selection posits that female mating preferences are by-products of natural selection on sensory systems. Although sensory bias was proposed 20 years ago, its critical assumptions remain untested. This paradox arises because sensory bias has been used to explain two different phenomena. First, it has been used as a hypothesis about signal design, that is, that males evolve traits that stimulate female sensory systems. Second, sensory bias has been used as a hypothesis for the evolution of female preference itself, that is, to explain why females exhibit particular preferences. We focus on this second facet. First, we clarify the unique features of sensory bias relative to the alternative models by considering each in the same quantitative genetic framework. The key assumptions of sensory bias are that natural selection is the predominant evolutionary mechanism that affects preference and that sexual selection on preferences is quantitatively negligible. We describe four studies that would test these assumptions and review what we can and cannot infer about sensory bias from existing studies. We suggest that the importance of sensory bias as an explanation for the evolution of female preferences remains to be determined.     

Foraging costs drive female resistance to a sensory trap

Male ornaments can evolve through the exploitation of female perceptual biases such as those involved in responding to cues from food. This type of sensory exploitation may lead to confusion between the male signals and the cues that females use to find/recognize food. Such interference would be costly to females and may be one reason why females evolve resistance to the male ornaments. Using a group of species of viviparous fish where resistance to a sensory trap has evolved, we demonstrate that females exposed to an ornament that resembles food have a diminished foraging efficiency, that this effect is apparent when foraging on a food item with which the ornament shares visual attributes, and that not all species are equally affected by such confusion. Our results lend support to the model of ornamental evolution through chase-away sexual conflict.     

Cultural evolution and perpetuation of arbitrary communicative conventions in experimental microsocieties

Previous studies have shown that iconic graphical signs can evolve into symbols through repeated usage within dyads and interacting communities. Here we investigate the evolution of graphical signs over chains of participants. In these chains (or “replacement microsocieties”), membership of an interacting group changed repeatedly such that the most experienced members were continually replaced by naïve participants. Signs rapidly became symbolic, such that they were mutually incomprehensible across experienced members of different chains, and new entrants needed to learn conventionalised meanings. An objective measure of graphical complexity (perimetric complexity) showed that the signs used within the microsocieties were becoming progressively simplified over successive usage. This is the first study to show that the signs that evolve in graphical communication experiments can be transmitted to, and spontaneously adopted by, naïve participants. This provides critical support for the view that human communicative symbols could have evolved culturally from iconic representations.     

The value of teaching increases with tool complexity in cumulative cultural evolution

Human cumulative cultural evolution (CCE) is recognized as a powerful ecological and evolutionary force, but its origins are poorly understood. The long-standing view that CCE requires specialized social learning processes such as teaching has recently come under question, and cannot explain why such processes evolved in the first place. An alternative, but largely untested, hypothesis is that these processes gradually coevolved with an increasing reliance on complex tools. To address this, we used large-scale transmission chain experiments (624 participants), to examine the role of different learning processes in generating cumulative improvements in two tool types of differing complexity. Both tool types increased in efficacy across experimental generations, but teaching only provided an advantage for the more complex tools. Moreover, while the simple tools tended to converge on a common design, the more complex tools maintained a diversity of designs. These findings indicate that the emergence of cumulative culture is not strictly dependent on, but may generate selection for, teaching. As reliance on increasingly complex tools grew, so too would selection for teaching, facilitating the increasingly open-ended evolution of cultural artefacts.     

Evolution of social learning does not explain the origin of human cumulative culture

Because culture requires transmission of information between individuals, thinking about the origin of culture has mainly focused on the genetic evolution of abilities for social learning. Current theory considers how social learning affects the adaptiveness of a single cultural trait, yet human culture consists of the accumulation of very many traits. Here we introduce a new modeling strategy that tracks the adaptive value of many cultural traits, showing that genetic evolution favors only limited social learning owing to the accumulation of maladaptive as well as adaptive culture. We further show that culture can be adaptive, and refined social learning can evolve, if individuals can identify and discard maladaptive culture. This suggests that the evolution of such "adaptive filtering" mechanisms may have been crucial for the birth of human culture.     

Symbiogenesis,natural selection,and the dynamic Earth

One century ago, Constantin S. Mereschkowsky introduced the symbiogenesis theory for the origin of chloroplasts from ancient cyanobacteria which was later supplemented by Ivan E. Wallin’s proposal that mitochondria evolved from once free-living bacteria. Today, this Mereschkowsky–Wallin principle of symbiogenesis, which is also known as the serial primary endosymbiosis theory, explains the evolutionary origin of eukaryotic cells and hence the emergence of all eukaryotes (protists, fungi, animals and plants). In 1858, the concept of natural selection was described independently by Charles Darwin and Alfred R. Wallace. In the same year, Antonio Snider-Pellegrini proposed the idea of shifting continents, which was later expanded by Alfred Wegener, who published his theory of continental drift eight decades ago. Today, directional selection is accepted as the major cause of adaptive evolution within natural populations of micro- and macro-organisms and the theory of the dynamic Earth (plate tectonics) is well supported. In this article, I combine the processes and principles of symbiogenesis, natural selection and the dynamic Earth and propose an integrative ‘synade-model’ of macroevolution which takes into account organisms from all five Kingdoms of life.     

On the nature of cultural transmission networks: evidence from Fijian villages for adaptive learning biases

Unlike other animals, humans are heavily dependent on cumulative bodies of culturally learned information. Selective processes operating on this socially learned information can produce complex, functionally integrated, behavioural repertoires-cultural adaptations. To understand such non-genetic adaptations, evolutionary theorists propose that (i) natural selection has favoured the emergence of psychological biases for learning from those individuals most likely to possess adaptive information, and (ii) when these psychological learning biases operate in populations, over generations, they can generate cultural adaptations. Many laboratory experiments now provide evidence for these psychological biases. Here, we bridge from the laboratory to the field by examining if and how these biases emerge in a small-scale society. Data from three cultural domains-fishing, growing yams and using medicinal plants-show that Fijian villagers (ages 10 and up) are biased to learn from others perceived as more successful/knowledgeable, both within and across domains (prestige effects). We also find biases for sex and age, as well as proximity effects. These selective and centralized oblique transmission networks set up the conditions for adaptive cultural evolution.     

Paleolithic public goods games: why human culture and cooperation did not evolve in one step

It is widely agreed that humans have specific abilities for cooperation and culture that evolved since their split with their last common ancestor with chimpanzees. Many uncertainties remain, however, about the exact moment in the human lineage when these abilities evolved. This article argues that cooperation and culture did not evolve in one step in the human lineage and that the capacity to stick to long-term and risky cooperative arrangements evolved before properly modern culture. I present evidence that Homo heidelbergensis became increasingly able to secure contributions form others in two demanding Paleolithic public good games (PPGGs): cooperative feeding and cooperative breeding. I argue that the temptation to defect is high in these PPGGs and that the evolution of human cooperation in Homo heidelberngensis is best explained by the emergence of modern-like abilities for inhibitory control and goal maintenance. These executive functions are localized in the prefrontal cortex and allow humans to stick to social norms in the face of competing motivations. This scenario is consistent with data on brain evolution that indicate that the largest growth of the prefrontal cortex in human evolution occurred in Homo heidelbergensis and was followed by relative stasis in this part of the brain. One implication of this argument is that subsequent behavioral innovations, including the evolution of symbolism, art, and properly cumulative culture in modern Homo sapiens, are unlikely to be related to a reorganization of the prefrontal cortex, despite frequent claims to the contrary in the literature on the evolution of human culture and cognition.     

Playing with language,creating complexity: Has play contributed to the evolution of complex language?

We argue that enhanced play may have contributed to the emergence of complex language systems in modern humans (Homo sapiens). To support this idea, we first discuss evidence for an expansion of playing behavior connected to the extended childhood of modern human children, and the potential of this period for the transmission of complex cultural traits, including language. We then link two of the most important functions of play—exploration and innovation—to the potential for cumulative cultural evolution in general and for the emergence of complex language in particular. If correct, the shorter childhood of Neanderthals—involving restrictions on time to experiment and innovate—may have restricted their language (and other symbolic) system/s. Consequently, fully investigating the role that play may have had in the transmission of language and the development of symbolic cultures in both modern humans and Neanderthals provides a new avenue of research for Paleolithic archaeology and related disciplines.     

Five Misunderstandings About Cultural Evolution

Recent debates about memetics have revealed some widespread misunderstandings about Darwinian approaches to cultural evolution. Drawing from these debates, this paper disputes five common claims: (1) mental representations are rarely discrete, and therefore models that assume discrete, gene-like particles (i.e., replicators) are useless; (2) replicators are necessary for cumulative, adaptive evolution; (3) content-dependent psychological biases are the only important processes that affect the spread of cultural representations; (4) the “cultural fitness” of a mental representation can be inferred from its successful transmission; and (5) selective forces only matter if the sources of variation are random. We close by sketching the outlines of a unified evolutionary science of culture.

Evolution of the Ainu Language in Space and Time

Languages evolve over space and time. Illuminating the evolutionary history of language is important because it provides a unique opportunity to shed light on the population history of the speakers. Spatial and temporal aspects of language evolution are particularly crucial for understanding demographic history, as they allow us to identify when and where the languages originated, as well as how they spread across the globe. Here we apply Bayesian phylogeographic methods to reconstruct spatiotemporal evolution of the Ainu language: an endangered language spoken by an indigenous group that once thrived in northern Japan. The conventional dual-structure model has long argued that modern Ainu are direct descendants of a single, Pleistocene human lineage from Southeast Asia, namely the Jomon people. In contrast, recent evidence from archaeological, anthropological and genetic evidence suggest that the Ainu are an outcome of significant genetic and cultural contributions from Siberian hunter-gatherers, the Okhotsk, who migrated into northern Hokkaido around 900–1600 years ago. Estimating from 19 Ainu language varieties preserved five decades ago, our analysis shows that they are descendants of a common ancestor who spread from northern Hokkaido around 1300 years ago. In addition to several lines of emerging evidence, our phylogeographic analysis strongly supports the hypothesis that recent expansion of the Okhotsk to northern Hokkaido had a profound impact on the origins of the Ainu people and their culture, and hence calls for a refinement to the dual-structure model.     

A sensory bias has triggered the evolution of egg-spots in cichlid fishes

Although, generally, the origin of sex-limited traits remains elusive, the sensory exploitation hypothesis provides an explanation for the evolution of male sexual signals. Anal fin egg-spots are such a male sexual signal and a key characteristic of the most species-rich group of cichlid fishes, the haplochromines. Males of about 1500 mouth-brooding species utilize these conspicuous egg-dummies during courtship--apparently to attract females and to maximize fertilization success. Here we test the hypothesis that the evolution of haplochromine egg-spots was triggered by a pre-existing bias for eggs or egg-like coloration. To this end, we performed mate-choice experiments in the basal haplochromine Pseudocrenilabrus multicolor, which manifests the plesiomorphic character-state of an egg-spot-less anal fin. Experiments using computer-animated photographs of males indeed revealed that females prefer images of males with virtual ('in-silico') egg-spots over images showing unaltered males. In addition, we tested for color preferences (outside a mating context) in a phylogenetically representative set of East African cichlids. We uncovered a strong preference for yellow, orange or reddish spots in all haplochromines tested and, importantly, also in most other species representing more basal lines. This pre-existing female sensory bias points towards high-quality (carotenoids-enriched) food suggesting that it is adaptive.     

Mimicry for all modalities

Mimicry is a canonical example of adaptive signal design. In principle, what constitutes mimicry is independent of the taxonomic identity of the mimic, the ecological context in which it operates, and the sensory modality through which it is expressed. However, in practice the study of mimicry is inconsistent across research fields, with theoretical and empirical advances often failing to cross taxonomic and sensory divides. We propose a novel conceptual framework whereby mimicry evolves if a receiver perceives the similarity between a mimic and a model and as a result confers a selective benefit onto the mimic. Here, misidentification and/or deception are no longer formal requirements, and mimicry can evolve irrespective of the underlying proximate mechanisms. The centrality of receiver perception in this framework enables us to formally distinguish mimicry from perceptual exploitation and integrate mimicry and multicomponent signalling theory for the first time. In addition, it resolves inconsistencies in our understanding of the role of learning in mimicry evolution, and shows that imperfect mimicry is expected to be the norm. Mimicry remains a key model for understanding signal evolution and cognition, and we recommend the adoption of a unified approach to stimulate future interdisciplinary developments in this fascinating area of research.     

Culture and the evolution of obesity

Human predispositions to fatness and obesity are best understood in the context of cultural and biological evolution. Both genes and cultural traits that were adaptive in the context of past food scarcities play a role today in the etiology of maladaptive adult obesity. The etiology of obesity must account for the social distribution of the condition with regard to gender, ethnicity, social class, and economic modernization. This distribution, which has changed throughout history, undoubtedly involves cultural factors. A model of culture is presented that has advantages over an undifferentiated concept of the “environment” for hypothesis generation. Cultural predispositions to obesity are found in the productive economy, the mode of reproduction, social structure, and cultural beliefs about food and ideal body size. Cross-cultural comparison can contribute to an understanding of the prevalence of obesity in some modern affluent societies.     

Vision as temporal trace

Most current models of human and animal vision assume that the processes of vision involve 2D (or even 3D) internal representations of the external world--an iconic representation. Within these models, recognition involves some form of lineal, areal or volumetric comparison of these internal representations (either learned or innate) with current sensory inputs. However, this view has recently come under criticism. In this paper, a neural model of vision is explored in which this iconic world view is replaced by a temporally ordered trace of (essentially) local features. The model employs hierarchical, recurrently linked, self-organizing topological maps.     

Evolution of egg dummies in Tanganyikan cichlid fishes: the roles of parental care and sexual selection

Sexual selection has been suggested to be an important driver of speciation in cichlid fishes of the Great Lakes of Africa, and the presence of male egg dummies is proposed to have played a key role. Here, we investigate how mouthbrooding and egg dummies have evolved in Tanganyikan cichlids, the lineage which seeded the other African radiations, with a special emphasis on the egg dummies. Using modern phylogenetic comparative analyses and a phylogeny including 86% of the 200 described species, we provide formal evidence demonstrating correlated evolution between mouthbrooding and egg dummies in Tanganyikan cichlids. These results concur with existing evidence, suggesting that egg dummies have evolved through sensory exploitation. We also demonstrate that there is a strong evolutionary correlation between the presence of egg dummies and both pre‐ and post‐copulatory sexual selection. Moreover, egg dummy evolution was contingent on the intensity of pre‐ and post‐copulatory sexual selection in Tanganyikan cichlids. In sum, our results provide evidence supporting the hypothesis of egg dummies evolving through sensory exploitation and highlight the role of sexual selection in favouring the evolution and maintenance of this trait.     

Sex against virulence: the coevolution of parasitic diseases

Reciprocal selection is the underlying mechanism for host-parasite coevolutionary arms races. Its driving force is the reduction of host lifespan or fecundity that is caused by a parasite. Parasites evolve to optimize host exploitation, while hosts evolve to minimize the 'parasite-induced' loss of fitness (virulence). Research on the evolution of virulence has mostly emphasized the role of parasite evolution in determining virulence. However, host evolution, accelerated by sexual recombination, contributes to the evolution and expression of virulence as well. The Red Queen hypothesis predicts that genetic variation among host offspring facilitates selection for reduced virulence. Here, we outline a synthesis between current thinking about the evolution of virulence and the evolution of sex.