Sexual selection: Another Darwinian process

Why was sexual selection so important to Darwin? And why was it de-emphasized by almost all of Darwin's followers until the second half of the 20th century? These two questions shed light on the complexity of the scientific tradition named “Darwinism”. Darwin's interest in sexual selection was almost as old as his discovery of the principle of natural selection. From the beginning, sexual selection was just another “natural means of selection”, although different from standard “natural selection” in its mechanism. But it took Darwin 30 years to fully develop his theory, from the early notebooks to the 1871 book The Descent of Man, and Selection in Relation to Sex. Although there is a remarkable continuity in his basic ideas about sexual selection, he emphasized increasingly the idea that sexual selection could oppose the action of natural selection and be non adaptive. In time, he also gave more weight to mate choice (especially female choice), giving explicit arguments in favor of psychological notions such as “choice” and “aesthetic sense”. But he also argued that there was no strict demarcation line between natural and sexual selection, a major difficulty of the theory from the beginning. Female choice was the main reason why Alfred Russel Wallace, the co-discoverer of the principle of natural selection, engaged in a major controversy with Darwin about sexual selection. Wallace was suspicious about sexual selection in general, trying to minimize it by all sorts of arguments. And he denied entirely the existence of female choice, because he thought that it was both unnecessary and an anthropomorphic notion. This had something to do with his spiritualist convictions, but also with his conception of natural selection as a sufficient principle for the evolutionary explanation of all biological phenomena (except for the origin of mind). This is why Wallace proposed to redefine Darwinism in a way that excluded Darwin's principle of sexual selection. The main result of the Darwin–Wallace controversy was that most Darwinian biologists avoided the subject of sexual selection until at least the 1950 s, Ronald Fisher being a major exception. This controversy still deserves attention from modern evolutionary biologists, because the modern approach inherits from both Darwin and Wallace. The modern approach tends to present sexual selection as a special aspect of the theory of natural selection, although it also recognizes the big difficulties resulting from the inevitable interaction between these two natural processes of selection. And contra Wallace, it considers mate choice as a major process that deserves a proper evolutionary treatment. The paper's conclusion explains why sexual selection can be taken as a test case for a proper assessment of “Darwinism” as a scientific tradition. Darwin's and Wallace's attitudes towards sexual selection reveal two different interpretations of the principle of natural selection: Wallace's had an environmentalist conception of natural selection, whereas Darwin was primarily sensitive to the element of competition involved in the intimate mechanism of any natural process of selection. Sexual selection, which can lack adaptive significance, reveals this exemplarily.     

1 July 1858: what Wallace knew; what Lyell thought he knew; what both he and Hooker took on trust; and what Charles Darwin never told them

At the Linnean Society on 1 July 1858, Charles Lyell and Joseph Hooker, using only an extract from Charles Darwin's unpublished essay of 1844, and a copy of a recent letter to Asa Gray in Boston, argued successfully that Darwin understood how species originate long before a letter from Alfred Russel Wallace outlining his own version of the theory of evolution arrived at Darwin's home. That letter from Ternate in the Malay Archipelago, however, was not the first letter Darwin received from Wallace. This article will contend that two of the three letters Wallace sent Darwin between 10 October 1856 and 9 March 1858 arrived much earlier than Darwin recorded, thereby allowing him time to assess Wallace's ideas and claim an independent understanding of how the operation of divergence and extinction in the natural world leads strongly marked varieties to be identified as new species. By the time of the Linnean meeting Darwin's new ideas had filtered into his letters and ‘big’ species book, despite the absence of any independent evidence from the natural world to justify his constant insistence to have been guided only by inductive reasoning. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 725–736.     

Patrick Matthew's law of natural selection

Patrick Matthew is the little‐known first originator of macroevolution by natural selection. I review his ideas, and introduce some previously unnoticed writings (catalogued at a new website: http://smarturl.it/patrickmatthew ) that clarify how they differ from Darwin's and Wallace's. Matthew's formulation emphasized natural selection as an axiomatic ‘law’ rather than a ‘theory’, a distinction that could still be of use to us today. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ●● , ●●–●●.     

How Charles Darwin received Wallace's Ternate paper 15 days earlier than he claimed: a comment on van Wyhe and Rookmaaker (2012)

Van Wyhe and Rookmaaker (2012) postulate a set of events to support their claim that Wallace's ‘evolution’ letter, posted at Ternate in the Moluccas in the spring of 1858, arrived at Darwin's home on 18 June 1858. If their claim were to be proven, then evidence that Darwin probably received Wallace's letter 2 weeks earlier than he ever admitted would clearly be erroneous, and any charges that he plagiarized the ideas of Wallace from that letter would be shown to be wrong. Here, evidence against this interpretation is presented and it is argued that the letter did indeed arrive in the port of Southampton on 2 June 1858 and would have been at Darwin's home near London the following day. If this were true, then the 66 new pages of material on aspects of Divergence that Darwin entered into his ‘big’ species book in the weeks before admitting he had received the letter could be interpreted as an attempt to present Wallace's ideas as his own. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 472–477.     

Engaging with Lyell: Alfred Russel Wallace’s Sarawak Law and Ternate papers as reactions to Charles Lyell’s Principles of Geology

Alfred Russel Wallace (1823–1913) and Charles Darwin (1809–1882) are honored as the founders of modern evolutionary biology. Accordingly, much attention has focused on their relationship, from their independent development of the principle of natural selection to the receipt by Darwin of Wallace’s essay from Ternate in the spring of 1858, and the subsequent reading of the Wallace and Darwin papers at the Linnean Society on 1 July 1858. In the events of 1858 Wallace and Darwin are typically seen as central players, with Darwin’s friends Charles Lyell (1797–1875) and Joseph Dalton Hooker (1817–1911) playing supporting roles. This narrative has resulted in an under-appreciation of a more central role for Charles Lyell as both Wallace’s inspiration and foil. The extensive anti-transmutation arguments in Lyell’s landmark Principles of Geology were taken as the definitive statement on the subject. Wallace, in his quest to solve the mystery of species origins, engaged with Lyell’s arguments in his private field notebooks in a way that is concordant with his engagement with Lyell in the 1855 and 1858 papers. I show that Lyell was the object of Wallace’s Sarawak Law and Ternate papers through a consideration of the circumstances that led Wallace to send his Ternate paper to Darwin, together with an analysis of the material that Wallace drew upon from the Principles. In this view Darwin was, ironically, intended for a supporting role in mediating Wallace’s attempted dialog with Lyell.     

Perspectives Poulton,Wallace and Jordan: How discoveries in Papilio butterflies led to a new species concept 100 years ago

A hundred years ago, in January 1904, E.B. Poulton gave an address entitled ‘What is a species?’ The resulting article, published in the Proceedings of the Entomological Society of London, is perhaps the first paper ever devoted entirely to a discussion of species concepts, and the first to elaborate what became known as the ‘biological species concept’. Poulton argued that species were syngamic (i.e. formed reproductive communities), the individual members of which were united by synepigony (common descent). Poulton's species concept was informed by his knowledge of polymorphic mimicry in Papilio butterflies: male and female forms were members of the same species, in spite of being quite distinct morphologically, because they belonged to syngamic communities. It is almost certainly not a coincidence that Alfred Russel Wallace had just given Poulton a book on mimicry in December 1903. This volume contained key reprints from the 1860s including the first mimicry papers, by Henry Walter Bates, Wallace himself and Roland Trimen. All these papers deal with species concepts and speciation as well as mimicry, and the last two contain the initial discoveries about mimetic polymorphism in Papilio: strongly divergent female morphs must belong to the same species as non‐mimetic males, because they can be observed in copula in nature. Poulton, together with his contemporaries Karl Jordan and Walter Rothschild, who had monographed world Papilionidae, were strongly influential on the evolutionary synthesis 40 years later. Ernst Mayr, in particular, had collected birds and butterflies for Walter Rothschild, and had visited Tring, where Jordan worked, in the 1920s. The recognition of different kinds of reproductive and geographic isolation, the classification of isolating mechanisms, the use of the term sympatry, and the biological species concept all trace back to Poulton's 1904 paper. Poulton's paper, in turn, inherits much from Wallace's 1865 paper on Asian Papilio contained in the very book Wallace gave Poulton a month earlier. Wallace's gift, and Poulton's subsequent New Year address are thus key events in the history of species concepts, systematics and evolutionary biology.     

More on the genetical theory of multilevel selection

In my article The genetical theory of multilevel selection, I provided a synthesis of the theory of multilevel selection (MLS) and the theory of natural selection in class‐structured populations. I framed this synthesis within Fisher's genetical paradigm, taking a strictly genetical approach to traits and fitness. I showed that this resolves a number of long‐standing conceptual problems that have plagued the MLS literature, including the issues of ‘aggregate’ vs. ‘emergent’ group traits, ‘collective fitness₁’ vs. ‘collective fitness₂’ and ‘MLS1’ vs. ‘MLS2 ‘. In his commentary, Goodnight suggests this theoretical and conceptual synthesis is flawed in several respects. Here, I show this is incorrect, by: reiterating the theoretical and conceptual goals of my synthesis; clarifying that my genetical approach to traits is necessary for a proper analysis of the action of MLS independently of non‐Darwinian factors; emphasizing that the Price–Hamilton approach to MLS provides a consistent, useful and conceptually superior theoretical framework; and explaining the role of reproductive value in the study of natural selection in class‐structured populations. I also show that Goodnight's contextual analysis treatment of MLS in a class‐structured population is mathematically, biologically and conceptually inadequate.     

ENHANCING EVOLUTION AND ENHANCING EVOLUTION

It has been claimed in several places that the new genetic technologies allow humanity to achieve in a generation or two what might take natural selection hundreds of millennia in respect of the elimination of certain diseases and an increase in traits such as intelligence. More radically, it has been suggested that those same technologies could be used to instil characteristics that we might reasonably expect never to appear due to natural selection alone. John Harris, a proponent of this genomic optimism, claims in his book Enhancing Evolution that we not only have it in our power to enhance evolution, but that we also have a duty to do so. In this paper, I claim that Harris' hand is strong but that he overplays it nevertheless. He is correct to dismiss the arguments of the anti‐enhancement lobby and correct to say that enhancement is permissible; but ‘good’ is different from ‘permissible’ and his argument for the goodness of enhancement is less convincing. Moreover, he is simply wrong to claim that it generates a duty to enhance.     

Alfred Russel Wallace

Alfred Russel Wallace The British naturalist Alfred Russel Wallace (1823–1913), well known as co‐discoverer of the “Darwinian” principle of natural selection, came from an ordinary background. Wallace left school aged 14 and never attended University. He became a land surveyor and studied, in his spare time, the works of the most famous naturalists of his age. After extensive expeditions (Amazon, 1848–1852; Southeast Asia, 1854–1862), Wallace spent the rest of his life in England as a free‐lance science writer. His contributions to systematics (he discovered/described many new species), evolutionary biology, zoogeography, anthropology and other branches of the live sciences are summarized in his 22 books and ca. 700 papers. Since Wallace became an adherent of spiritualism and mixed up supernatural phenomena with scientific facts in some of his later books, he remains a controversial figure in the history of the life sciences.     

Darwin's error? Patrick Matthew and the catastrophic nature of the geologic record

In 1831, the Scottish horticulturalist Patrick Matthew (1790–1874) published a clear statement of the law of natural selection in an Appendix to his book Naval Timber and Arboriculture, which both Darwin and Wallace later acknowledged. Matthew, however, was a catastrophist, and he presented natural selection within the contemporary view that relatively long intervals of environmental stability were episodically punctuated by catastrophic mass extinctions of life. Modern studies support a similar picture of the division of geologic time into long periods of relative evolutionary stability ended by sudden extinction events. Mass extinctions are followed by recovery intervals during which surviving taxa radiate into vacated niches. This modern punctuated view of evolution and speciation is much more in line with Matthew's episodic catastrophism than the classical Lyellian–Darwinian gradualist view.     

The prominent absence of Alfred Russel Wallace at the Darwin anniversaries in Germany in 1909, 1959 and 2009

It is well known that the contribution of Alfred Russell Wallace (1823–1913) to the development of the “Darwinian” principle of natural selection has often been neglected. Here we focus on how the three anniversaries to celebrate the origin of the Darwin–Wallace theory in Germany in 1909, in 1959 in the divided country, as well as in 2009, have represented Charles Robert Darwin’s and Alfred Russell Wallace’s contributions. We have analyzed books and proceedings volumes related to these anniversaries, and the main result is that Wallace was almost always ignored, or only mentioned in passing. In 1909, Ernst Haeckel gave a talk in Jena, later published under the title The worldview of Darwin and Lamarck (Das Weltbild von Darwin und Lamarck), but not as the Darwin–Wallace concept. Haeckel mentions Wallace only once. In two important proceedings volumes from the 1959 anniversaries, Wallace was ignored. The only fair treatment of Wallace is given in another book, a collection of documents edited by Gerhard Heberer, for which the author selected nine key documents and reprinted excerpts (1959). Three of them were articles by Wallace, including the Sarawak- and Ternate-papers of 1855 and 1858, respectively. An analysis of the dominant themes during the celebrations of 2009 shows that none of the six topics had much to do with Wallace and his work. Thus, the tendency to exclude Alfred Russell Wallace is an international phenomenon, and largely attributable to the “Darwin industry”.     

A further look at the 1858 Wallace–Darwin mail delivery question

Recent investigations have led to a conclusion that Alfred Russel Wallace probably mailed his ‘Ternate’ paper on natural selection to Darwin 1 month later than some have assumed, thus freeing Darwin from possible accusations of plagiarism. Further examination of the question suggests that this conclusion is premature because the evidence in favour of the later mailing date appears to be weaker than first considered. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Suspending disbelief—of Wynne-Edwards and his reception

Critique of Wynne-Edwards' views on population regulation and sociality suppose a population of discrete, mutually exclusive groups essential to his thought. Yet both his past and present work focus on continually distributed, philopatric populations; his critics have argued the untenability of a position never his own. Wynne-Edwardsian ‘group selection’ focuses on local population productivity under philopatry. A ‘group’ is a local confluence of genotypes which need not be reified, and group selection consists of the differential replication (hence heritability) of the local social environment in which a genotype is embedded. Differential productivity contingent on social environment can eliminate some relational structures on genotypes in favor of others, creating an expanding wave of population productivity as in Wright's shifting balance metaphor. Such a process is inherent in the evolution of reciprocity, where cooperators must cluster to successfully invade a population of defectors. Regulation of resource exploitation in continuously distributed populations may be modeled as overlapping n-person Prisoner's Dilemmas, where each individual participates in several distinct commons and defection represents local over-exploitation of resources.     

Sexual selection in fungi

The significance of sexual selection, the component of natural selection associated with variation in mating success, is well established for the evolution of animals and plants, but not for the evolution of fungi. Even though fungi do not have separate sexes, most filamentous fungi mate in a hermaphroditic fashion, with distinct sex roles, that is, investment in large gametes (female role) and fertilization by other small gametes (male role). Fungi compete to fertilize, analogous to ‘male‐male’ competition, whereas they can be selective when being fertilized, analogous to female choice. Mating types, which determine genetic compatibility among fungal gametes, are important for sexual selection in two respects. First, genes at the mating‐type loci regulate different aspects of mating and thus can be subject to sexual selection. Second, for sexual selection, not only the two sexes (or sex roles) but also the mating types can form the classes, the members of which compete for access to members of the other class. This is significant if mating‐type gene products are costly, thus signalling genetic quality according to Zahavi's handicap principle. We propose that sexual selection explains various fungal characteristics such as the observed high redundancy of pheromones at the B mating‐type locus of Agaricomycotina, the occurrence of multiple types of spores in Ascomycotina or the strong pheromone signalling in yeasts. Furthermore, we argue that fungi are good model systems to experimentally study fundamental aspects of sexual selection, due to their fast generation times and high diversity of life cycles and mating systems.     

The Handicap Principle: how an erroneous hypothesis became a scientific principle

The most widely cited explanation for the evolution of reliable signals is Zahavi's so‐called Handicap Principle, which proposes that signals are honest because they are costly to produce. Here we provide a critical review of the Handicap Principle and its theoretical development. We explain why this idea is erroneous, and how it nevertheless became widely accepted as the leading explanation for honest signalling. In 1975, Zahavi proposed that elaborate secondary sexual characters impose ‘handicaps’ on male survival, not due to inadvertent signalling trade‐offs, but as a mechanism that functions to demonstrate males' genetic quality to potential mates. His handicap hypothesis received many criticisms, and in response, Zahavi clarified his hypothesis and explained that it assumes that signals are wasteful as well as costly, and that they evolve because wastefulness enforces honesty. He proposed that signals evolve under ‘signal selection’, a non‐Darwinian type of selection that favours waste rather than efficiency. He maintained that the handicap hypothesis provides a general principle to explain the evolution of all types of signalling systems, i.e. the Handicap Principle. In 1977, Zahavi proposed a second hypothesis for honest signalling, which received many different labels and interpretations, although it was assumed to be another example of handicap signalling. In 1990, Grafen published models that he claimed vindicated Zahavi's Handicap Principle. His conclusions were widely accepted and the Handicap Principle subsequently became the dominant paradigm for explaining the evolution of honest signalling in the biological and social sciences. Researchers have subsequently focused on testing predications of the Handicap Principle, such as measuring the absolute costs of honest signals (and using energetic and other proximate costs as proxies for fitness), but very few have attempted to test Grafen's models. We show that Grafen's models do not support the handicap hypothesis, although they do support Zahavi's second hypothesis, which proposes that males adjust their investment into the expression of their sexual signals according to their condition and ability to bear the costs (and risks to their survival). Rather than being wasteful over‐investments, honest signals evolve in this scenario because selection favours efficient and optimal investment into signal expression and minimizes signalling costs. This idea is very different from the handicap hypothesis, but it has been widely misinterpreted and equated to the Handicap Principle. Theoretical studies have since shown that signalling costs paid at the equilibrium are neither sufficient nor necessary to maintain signal honesty, and that honesty can evolve through differential benefits, as well as differential costs. There have been increasing criticisms of the Handicap Principle, but they have focused on the limitations of Grafen's model and overlooked the fact that it is not a handicap model. This model is better understood within a Darwinian framework of adaptive signalling trade‐offs, without the added burden and confusing logic of the Handicap Principle. There is no theoretical or empirical support for the Handicap Principle and the time is long overdue to usher this idea into an ‘honorable retirement’.     

The eunuch phenomenon: adaptive evolution of genital emasculation in sexually dimorphic spiders

Under natural and sexual selection traits often evolve that secure paternity or maternity through self‐sacrifice to predators, rivals, offspring, or partners. Emasculation—males removing their genitals—is an unusual example of such behaviours. Known only in insects and spiders, the phenomenon's adaptiveness is difficult to explain, yet its repeated origins and association with sexual size dimorphism (SSD) and sexual cannibalism suggest an adaptive significance. In spiders, emasculation of paired male sperm‐transferring organs — secondary genitals — (hereafter, palps), results in ‘eunuchs’. This behaviour has been hypothesized to be adaptive because (i) males plug female genitals with their severed palps (plugging hypothesis), (ii) males remove their palps to become better fighters in male–male contests (better‐fighter hypothesis), perhaps reaching higher agility due to reduced total body mass (gloves‐off hypothesis), and (iii) males achieve prolonged sperm transfer through severed genitals (remote‐copulation hypothesis). Prior research has provided evidence in support of these hypotheses in some orb‐weaving spiders but these explanations are far from general. Seeking broad macroevolutionary patterns of spider emasculation, we review the known occurrences, weigh the evidence in support of the hypotheses in each known case, and redefine more precisely the particular cases of emasculation depending on its timing in relation to maturation and mating: ‘pre‐maturation’, ‘mating’, and ‘post‐mating’. We use a genus‐level spider phylogeny to explore emasculation evolution and to investigate potential evolutionary linkage between emasculation, SSD, lesser genital damage (embolic breakage), and sexual cannibalism (females consuming their mates). We find a complex pattern of spider emasculation evolution, all cases confined to Araneoidea: emasculation evolved at least five and up to 11 times, was lost at least four times, and became further modified at least once. We also find emasculation, as well as lesser genital damage and sexual cannibalism, to be significantly associated with SSD. These behavioural and morphological traits thus likely co‐evolve in spiders. Emasculation can be seen as an extreme form of genital mutilation, or even a terminal investment strategy linked to the evolution of monogyny. However, as different emasculation cases in araneoid spiders are neither homologous nor biologically identical, and may or may not serve as paternity protection, the direct link to monogyny is not clear cut. Understanding better the phylogenetic patterns of emasculation and its constituent morphologies and behaviours, a clearer picture of the intricate interplay of natural and sexual selection may arise. With the here improved evolutionary resolution of spider eunuch behaviour, we can more specifically tie the evidence from adaptive hypotheses to independent cases, and propose promising avenues for further research of spider eunuchs, and of the evolution of monogyny.     

Mating patterns influence vulnerability to the extinction vortex

Earth's biodiversity is undergoing mass extinction due to anthropogenic compounding of environmental, demographic and genetic stresses. These different stresses can trap populations within a reinforcing feedback loop known as the extinction vortex, in which synergistic pressures build upon one another through time, driving down population viability. Sexual selection, the widespread evolutionary force arising from competition, choice and reproductive variance within animal mating patterns could have vital consequences for population viability and the extinction vortex: (a) if sexual selection reinforces natural selection to fix ‘good genes’ and purge ‘bad genes’, then mating patterns encouraging competition and choice may help protect populations from extinction; (b) by contrast, if mating patterns create load through evolutionary or ecological conflict, then population viability could be further reduced by sexual selection. We test between these opposing theories using replicate populations of the model insect Tribolium castaneum exposed to over 10 years of experimental evolution under monogamous versus polyandrous mating patterns. After a 95‐generation history of divergence in sexual selection, we compared fitness and extinction of monogamous versus polyandrous populations through an experimental extinction vortex comprising 15 generations of cycling environmental and genetic stresses. Results showed that lineages from monogamous evolutionary backgrounds, with limited opportunities for sexual selection, showed rapid declines in fitness and complete extinction through the vortex. By contrast, fitness of populations from the history of polyandry, with stronger opportunities for sexual selection, declined slowly, with 60% of populations surviving by the study end. The three vortex stresses of (a) nutritional deprivation, (b) thermal stress and (c) genetic bottlenecking had similar impacts on fitness declines and extinction risk, with an overall sigmoid decline in survival through time. We therefore reveal sexual selection as an important force behind lineages facing extinction threats, identifying the relevance of natural mating patterns for conservation management.     

Broad‐scale variation in sexual dichromatism in songbirds is not explained by sex differences in exposure to predators during incubation

The evolution of sexual dichromatism provoked one of the greatest disagreements between Charles Darwin and Alfred Russel Wallace. According to Darwin the main driving force is sexual selection, whereby choosy females prefer showy males, leading to the evolution of conspicuous male plumage. On the other hand, Wallace suggested that dichromatism may arise because nest predation favors more cryptic females. To test the role of natural selection in the evolution of dichromatism we combined quantitative data on differences in parental share in nest attentiveness (representing the strength of natural selection on males vs females) with spectrophotometric measurements of dichromatism in 412 species of songbirds from 69 families. We expected to find stronger dichromatism in open‐nesting species with more divergent parental roles and in body parts exposed during incubation. Dichromatism was not related to the differences in parental share during incubation, but it was most pronounced in lekking species, migrants, and small species. Our results thus suggest that Wallace's hypothesis is not able to explain broad‐scale variation in the dichromatism of songbirds, but point to a role for sexual selection, mutual mate choice, and migration strategy in shaping the extraordinary variation in dichromatism exhibited by songbirds.     

Biological relativity to water–energy dynamics

Climate has long been related to geographical differences in the distribution and diversity of life. What has eluded explanation is why this should be so. One emerging possibility is biological relativity to water–energy dynamics: the relative nature of biotic dynamics to changes in energy/matter conditions caused by changes in water (all states) while doing work, especially liquid water. The dynamic parameters involved – liquid water and optimal energy conditions – are independent of life, and have been shown to provide a simple, globally predictive explanation for co‐variation between climate and the species richness of woody plants. Here I elaborate on what I mean by ‘biological relativity to water–energy dynamics’ and how it should relate to the geography and evolution of life in general (terrestrial, subterranean, marine/aquatic biota). Working through a natural hierarchy of physical, geographical, ecological and biological first principles, I outline the hierarchical, abiotic → biotic conceptual framework within which this idea operates. The implications of this idea include the following. First, the biosphere is better conceptualized as a ‘subsphere’ of the liquid hydrosphere – a system within a system, wherein ‘life’ has all the unique physical properties of liquid water, plus unique emergent properties of its own. Second, the fundamental capacity for life to exist and be dynamic in all biotic systems is determined by the abiotic capacity for liquid water to exist and be dynamic, which is always relative to the capacity for water–energy dynamics in general. Third, liquid water–energy dynamics acts as a fundamental mechanism of evolution, while being a constant mechanism of natural selection. Fourth, over space and time, there should be first‐order predictable and/or systematic differences in the capacity for, operation and outcomes of, biotic dynamics globally (e.g. species richness), that necessarily dissolve into apparent chaos locally. Fifth, biological relativity to water–energy dynamics provides a fundamental and natural framework for operationalizing hierarchy theory and developing trans‐scalar explanations for the geography and evolution of life's diversity.