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An Updated Theoretical Framework for Human Sexual Selection: from Ecology, Genetics, and Life History to Extended Phenotypes

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Abstract

Objectives

Sexual selection typically centers on bodily and psychological traits. Non-bodily traits ranging from housing and vehicles through art to social media can, however, influence sexual selection even in absence of the phenotype proper. The theoretical framework of human sexual selection is updated in this article by unifying four theoretical approaches and conceptualizing non-bodily traits as extended phenotypic traits.

Methods

Existing research is synthesized with extended phenotype theory, life history theory, and behavioral ecology. To test population-level hypotheses arising from the review, ecological and demographic data on 122 countries are analyzed with multiple linear regression modelling.

Results

A four-factor model of intelligence, adolescent fertility, population density, and atmospheric cold demands predicts 64% of global variation in economic complexity in 1995 and 72% of the variation in 2016.

Conclusions

The evolutionary pathways of extended phenotypes frequently undergo a categorical broadening from providing functional benefits to carrying signalling value. Extended phenotypes require investments in skills and bioenergetic resources, but they can improve survival in high latitudes, facilitate the extraction of resources from the environment, and substantially influence sexual selection outcomes. Bioenergetic investments in extended phenotypes create individual- and population-level tradeoffs with competing life history processes, exemplified here as a global tradeoff between adolescent fertility and economic complexity. The merits of the present model include a more systematic classification of sexual traits, a clearer articulation of their evolutionary-developmental hierarchy, and an analysis of ecological, genetic, and psychological mechanisms that modulate the flow of energy into extended phenotypes and cultural innovations.

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Notes

  1. Inherited wealth may be an exception. In a limited number of cases, the causal succession from a phenotype to behavior to extended phenotypes can potentially skip the intermediate step behavior.

  2. A possible exception may be fat tissue metabolized via excessive energy intake or muscle tissue growth stimulated by adaptations to physical work or exercise (Camera et al. 2016; Wells 2006).

  3. Equatorial distance is a proxy of climate: it correlates significantly (r = .90) with daily minimum temperature (IJzerman et al. 2017) and cold demands (r = .88, as described below).

  4. See Roth and Pravosudov (2009), Vincze (2016), and especially Fristoe et al. (2017), for similar results in bird species, as well as a discussion on direction of causality, which suggests that, in birds, it was brain expansion that led to the colonization of variable habitats rather than colonization of variable habitats leading to brain expansion.

  5. Brussels was chosen as a proxy for Europe’s central point for the present purposes since it is located between Europe’s geographical centre (Suchowola, Poland) and financial centre (London, UK) and constitutes the administrative centre of the European Union.

  6. Spearman’s rank correlation coefficient was used because of non-normal distribution of data for the variable coldest month.

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Acknowledgements

This work was supported by the Otto A. Malm foundation, The University of Auckland Doctoral Scholarship, and the Emil Aaltonen Young Researcher Grant. The author is grateful for Brian Boyd’s and Quentin Atkinson’s meticulous criticism, Markus J. Rantala’s guidance, and for Oliver Sheehan, Ania Grant, and Patrick Neilands for their valuable comments on earlier drafts. The author wishes to thank the University of Auckland Language, Culture and Cognition group for several thoughtful discussions on the topic. The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Glossary

Allele

each of two or more alternative forms of a gene found in the same genetic locus.

Atmospheric cold demands

a climatic variable that is coded as the sum of the absolute downward deviations from 22 °C for the average lowest temperature in the coldest month, the average highest temperature in the coldest month, the average lowest temperature in the hottest month, and the average highest temperature in the hottest month (Van de Vliert 2013).

Behavioral ecology

studies the evolutionary basis for behavior shaped by ecological pressures such as climate, habitat characteristics, and conspecific interactions.

Cognitive buffer hypothesis

suggests that the primary adaptive function of a large brain is to buffer individuals against environmental challenges by facilitating the construction of behavioral responses (Sol 2009).

Conspecifics

are members of the same species; heterospecifics are members of a different species.

Cues

can provide information to other organisms, but they were not evolutionarily selected for the specific purpose of conveying information. Many signals have nevertheless evolved from cues through the evolutionary process of signaller precursor route: signals can evolve from behaviors or structures that originally were informative aspects of the signaller and then became specialized over evolutionary time to convey information more effectively (Laidre and Johnstone 2013). It can be challenging to establish what is a cue and what is a signal (Sugiyama 2015) especially in contemporary human sexual selection on extended phenotypic traits. This is why the current work (mostly) refrains from discussing extended phenotypic traits as signals and instead refers to them simply as cues or traits.

Ecological inheritance

refers to ecological legacies passed on to future generations that are generated by niche construction activities of past generations.

Economic Complexity Index (ECI)

a holistic measure of the knowledge, industrial composition, and production characteristics of a country.

Exaptation

a feature that enhances fitness in a way that differs from its “original” evolutionarily selected role; i.e. it is a trait that currently has a positive fitness effect without being an adaptation specifically for that effect (Buss et al. 1998; Gould and Vrba 1982).

Extended phenotypes

are a part of the phenotype expressed beyond the body. In simplified terms, and not taking into account the polygenic architecture underlying the creation or manipulation of extended phenotypes, they result from the effects of an allele upon the world that have a bearing on that allele’s survival or proliferation (Dawkins 2004). This includes any feature of the abiotic or biotic environment that is the result of manipulative action or construction behavior of an individual, but excludes any result of such manipulative behavior that does not affect the organism’s fitness negatively or positively (Dawkins 1982; Schaedelin and Taborsky 2009). This definition therefore includes the dam that a beaver builds, but not the footprints it makes when building it (Dawkins 1982, p. 315). Both result from the action of an organism upon the world, but only the dam has a fitness implication to the beaver. Extended phenotypes can be divided into inanimate and animate ones.

Extended phenotypic plasticity

refers to the process of extended phenotypes adapting to the demands of the environment, interacting with it, and gaining feedback from it, thereby creating phenotype–environment interactions and extended phenotype–environment interactions that flow through generations (Blamires 2010; Lehmann 2008).

Functional traits

are the morphological, physiological, phenological, and behavioral characteristics of an organism that have an influence on performance or fitness (Meunier et al. 2017).

Kin selection

refers to any variation in indirect fitness among different phenotypes caused by their ability to influence the reproductive success and survival of genetically similar individuals.

Natural selection

is the sum total of viability selection, sexual selection, and kin selection (Cornwallis and Uller 2010).

Niche construction

is a theoretical framework that studies the ways in which organisms choose and modify components of their local environments.

Phenotype

is the composite of an organism’s observable physical or biochemical features (as determined by genetic makeup and environmental influences) (Bolondi et al. 2017). Cognitive traits such as intelligence are classified as phenotypic traits in this article. Thus, phenotypic traits can be further divided into somatic (physical) and cognitive (psychological) traits (e.g. Miller and Todd 1998). Much literature exists on behavioral phenotypes; for reasons of theoretical accuracy and empirical distinction, however, behavioral traits are here distinguished from phenotypic traits. Likewise, though extended phenotypic traits could be seen as a subcategory of phenotypic traits, they are treated as a separate category because they do not fulfil the orthodox definition of a phenotype.

Phenotypic plasticity

refers to the ability of a single genotype to produce multiple phenotypes when exposed to different environments.

Secondary adaptations

(sometimes called post-adaptations) are adaptive changes that an exaptation undergoes to become better suited to its evolutionarily novel function.

Secondary sexual signals

are sexually selected traits that give an organism an advantage over its rivals in mate choice without being directly involved in reproduction. Examples in humans include enlarged breasts and muscles.

Sexual selection

is defined as any variation in direct fitness among different phenotypes caused by their ability to gain sexual partners, produce fertilized eggs, and generate offspring.

Signals

are traits that were evolutionarily selected for because they conveyed information about the signaller, affecting the behavior of other organisms and ultimately impacting the fitness of both the signaller and the recipient (Laidre and Johnstone 2013).

Trait-based ecology

provides a functional approach to understanding ecological interactions by focusing on the expression of functional traits under distinct environmental conditions (Meunier et al. 2017).

Viability selection

refers to any variation in direct fitness among different phenotypes caused by their ability to survive.

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Luoto, S. An Updated Theoretical Framework for Human Sexual Selection: from Ecology, Genetics, and Life History to Extended Phenotypes. Adaptive Human Behavior and Physiology 5, 48–102 (2019). https://doi.org/10.1007/s40750-018-0103-6

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