Human breasts: Unsupported hypotheses reviewed

Unlike other apes, human females’ breasts develop before first pregnancy and are permanently enlarged. Evidence suggests breasts act as signals to males but the critical data required to confirm this are lacking. These facts have led to a number of hypotheses about the evolutionary and adaptive significance of the human breast which fall into two groups. Those that address the presence of breasts in humans are (a) that they act as releasers of male sexual behaviour, (b) that they enable females to hide their reproductive condition, and (c) that they allow infants to nurse from their mother’s hip. Those that address variability in breast size are (d) that large breasts indicate lactational potential, (e) ability of mothers to invest prenatally in offspring, (f) mother’s fecundity, and (g) her longevity. Each hypothesis is reviewed and evaluated using logical or empirical arguments. Possible ways in which the adaptive significance of human breasts can be determined in contemporary populations are outlined.     

Host fecundity reduction: a strategy for damage limitation?

Host fecundity reduction is a life-history trait that is commonly exhibited in parasitic associations. It is particularly prevalent in female invertebrate hosts that invest heavily in egg production during a relatively short life span. Here, Hilary Hurd uses examples of parasitized insects and trematode infections of snails to consider the evolutionary significance of this response to infection. Studies of host egg production and reports of the physiological mechanisms underlying reduction of host reproductive success are used to evaluate the hypotheses that fecundity reduction might be a by-product of infection, or an adaptive strategy on the part of parasite or host.     

The nubility hypothesis

A new hypothesis is proposed to explain the perennially enlarged breasts of human females. The nubility hypothesis proposes that hominid females evolved protruding breasts because the size and shape of breasts function as an honest signal of residual reproductive value. Hominid females with greater residual reproductive value were preferred by males once reliable cues to ovulation were lost and long-term bonding evolved. This adaptation was favored because female-female competition for investing males increased once hominid males began to provide valuable resources.     

A comparative method for studying adaptation to a randomly evolving environment

Most phylogenetic comparative methods used for testing adaptive hypotheses make evolutionary assumptions that are not compatible with evolution toward an optimal state. As a consequence they do not correct for maladaptation. The "evolutionary regression" that is returned is more shallow than the optimal relationship between the trait and environment. We show how both evolutionary and optimal regressions, as well as phylogenetic inertia, can be estimated jointly by a comparative method built around an Ornstein-Uhlenbeck model of adaptive evolution. The method considers a single trait adapting to an optimum that is influenced by one or more continuous, randomly changing predictor variables.     

The enduring puzzle of the human chin

Although modern humans are considered to be morphologically distinct from other living primates because of our large brains, dexterous hands, and bipedal gait, all of these features are found among extinct hominins. The chin, however, appears to be a uniquely modern human trait. Probably because of the chin's exclusivity, many evolutionary scenarios have been proposed to explain its origins. To date, researchers have developed adaptive hypotheses relating chins to speech, mastication, and sexual selection; still others see it as a structural artifact tangentially related to complex processes involving evolutionary retraction of the midfacial skeleton. Consensus has remained elusive, partly because hypotheses purporting to explain how this feature developed uniquely in modern humans are all fraught with theoretical and/or empirical shortcomings. Here we review a century's worth of chin hypotheses and discuss future research avenues that may provide greater insight into this human peculiarity.     

Asexual propagules as an adaptive trait for epiphylly in tropical leafy liverworts (Lejeuneaceae)

? Premise of the study: Many links between form and function are described in the context of adaptation. Several morphological and life-history traits in the leafy liverwort family Lejeuneaceae (Marchantiophyta) have been hypothesized to be adaptations for living on the surface of leaves of vascular plants (epiphylly). There have been, however, no rigorous tests of these hypotheses. ? Methods: Using a recently published phylogeny of Lejeuneaceae and trait data from published monographs, I tested the correlations of putative adaptive traits with the incidence of epiphylly. Both cross-species and phylogenetic-based analyses of trait data were performed to distinguish the patterns of shared evolutionary history from independent origins of putatively adaptive traits. The rates of transitions between different combinations of character states were also calculated to determine whether traits were more likely to evolve in the presence of epiphylly. ? Key results: Only one trait, production of asexual propagules, was correlated with epiphylly in the phylogenetic-based analysis. The rate of transition to asexual propagules was also significantly higher in the presence of epiphylly. Other traits correlated with epiphylly appeared to be the results of shared evolutionary history among sister taxa and therefore not due to adaptive evolution. ? Conclusion: The present study distinguished production of asexual propagules from other traits as a key adaptive response to living on the leaf surface. No other putative "adaptive" traits to epiphylly showed evidence of being specific adaptation to epiphylly. The results highlight the importance of phylogenetically controlled methods in determining an adaptive function of traits.     

A single origin of large colony size in allodapine bees suggests a threshold event among 50 million years of evolutionary tinkering

Evolutionary origins of highly eusocial organization involving morphological castes have been very rare, yet these origins have often led to enormous diversification and ecological success. This suggests that once an apparently severe selective barrier to highly eusocial behaviour is overcome, major new adaptive landscapes open up. One would therefore expect a discontinuity in patterns of evolutionary change across this barrier. However, we do not know if highly eusocial organization has evolved incrementally from less complex societies, or if it has involved some kind of evolutionary leap. Our study examines this issue using colony size data from 33 allodapine bee species, with a crown age of ca. 47 Mya. Our species cover all major allodapine clades, and include Exoneurella tridentata, the only known allodapine with morphologically discrete castes. Phylogenetic analyses indicate a strong effect of phylogeny on the evolution of maximum brood size, but the effect of phylogeny on maximum colony size (number of adults) depends on whether E. tridentata is excluded or included in analyses. We found no evidence of punctuational change in maximum colony or brood sizes over the phylogeny as a whole, but colony and brood sizes in E. tridentata fall well beyond variation among the other allodapines. Colony size in E. tridentata therefore represents an evolutionary outcome that does not fit within the kinds of incremental changes found in other allodapines. We propose that E. tridentata indicates the crossing of an important threshold, and this has entailed some very unusual ecological circumstances.     

The mechanistic,genetic and evolutionary causes of bird eye colour variation

Birds display a rainbow of eye colours, but this trait has been little studied compared with plumage coloration. Avian eye colour variation occurs at all phylogenetic scales: it can be conserved throughout whole families or vary within one species, yet the evolutionary importance of this eye colour variation is under-studied. Here, we summarize knowledge of the causes of eye colour variation at three primary levels: mechanistic, genetic and evolutionary. Mechanistically, we show that avian iris pigments include melanin and carotenoids, which also play major roles in plumage colour, as well as purines and pteridines, which are often found as pigments in non-avian taxa. Genetically, we survey classical breeding studies and recent genomic work on domestic birds that have identified potential ‘eye colour genes’, including one associated with pteridine pigmentation in pigeons. Finally, from an evolutionary standpoint, we present and discuss several hypotheses explaining the adaptive significance of eye colour variation. Many of these hypotheses suggest that bird eye colour plays an important role in intraspecific signalling, particularly as an indicator of age or mate quality, although the importance of eye colour may differ between species and few evolutionary hypotheses have been directly tested. We suggest that future studies of avian eye colour should consider all three levels, including broad-scale iris pigment analyses across bird species, genome sequencing studies to identify loci associated with eye colour variation, and behavioural experiments and comparative phylogenetic analyses to test adaptive hypotheses. By examining these proximate and ultimate causes of eye colour variation in birds, we hope that our review will encourage future research to understand the ecological and evolutionary significance of this striking avian trait.     

Genome biogeography reveals the intraspecific spread of adaptive mutations for a complex trait

Physiological novelties are often studied at macro‐evolutionary scales such that their micro‐evolutionary origins remain poorly understood. Here, we test the hypothesis that key components of a complex trait can evolve in isolation and later be combined by gene flow. We use C₄ photosynthesis as a study system, a derived physiology that increases plant productivity in warm, dry conditions. The grass Alloteropsis semialata includes C₄ and non‐C₄ genotypes, with some populations using laterally acquired C₄‐adaptive loci, providing an outstanding system to track the spread of novel adaptive mutations. Using genome data from C₄ and non‐C₄ A. semialata individuals spanning the species’ range, we infer and date past migrations of different parts of the genome. Our results show that photosynthetic types initially diverged in isolated populations, where key C₄ components were acquired. However, rare but recurrent subsequent gene flow allowed the spread of adaptive loci across genetic pools. Indeed, laterally acquired genes for key C₄ functions were rapidly passed between populations with otherwise distinct genomic backgrounds. Thus, our intraspecific study of C₄‐related genomic variation indicates that components of adaptive traits can evolve separately and later be combined through secondary gene flow, leading to the assembly and optimization of evolutionary innovations.     

Phycoerythrin evolution and diversification of spectral phenotype in marine Synechococcus and related picocyanobacteria

In marine Synechococcus there is evidence for the adaptive evolution of spectrally distinct forms of the major light harvesting pigment phycoerythrin (PE). Recent research has suggested that these spectral forms of PE have a different evolutionary history than the core genome. However, a lack of explicit statistical testing of alternative hypotheses or for selection on these genes has made it difficult to evaluate the evolutionary relationships between spectral forms of PE or the role horizontal gene transfer (HGT) may have had in the adaptive phenotypic evolution of the pigment system in marine Synechococcus. In this work, PE phylogenies of picocyanobacteria with known spectral phenotypes, including newly co-isolated strains of marine Synechococcus from the Gulf of Mexico, were constructed to explore the diversification of spectral phenotype and PE evolution in this group more completely. For the first time, statistical evaluation of competing evolutionary hypotheses and tests for positive selection on the PE locus in picocyanobacteria were performed. Genes for PEs associated with specific PE spectral phenotypes formed strongly supported monophyletic clades within the PE tree with positive directional selection driving evolution towards higher phycourobilin (PUB) content. The presence of the PUB-lacking phenotype in PE-containing marine picocyanobacteria from cyanobacterial lineages identified as Cyanobium is best explained by HGT into this group from marine Synechococcus. Taken together, these data provide strong examples of adaptive evolution of a single phenotypic trait in bacteria via mutation, positive directional selection and horizontal gene transfer.     

Territorial aggression and hormones during the non-breeding season in a tropical bird

The hormonal control of territorial aggression in male and female vertebrates outside the breeding season is still unresolved. Most vertebrates have regressed gonads when not breeding and do not secrete high levels of sex steroids. However, recent studies implicate estrogens in the regulation of non-breeding territoriality in some bird species. One possible source of steroids during the non-breeding season could be the adrenal glands that are known to produce sex steroid precursors such as dehydroepiandrosterone (DHEA). We studied tropical, year-round territorial spotted antbirds (Hylophylax n. naevioides) and asked (1). whether both males and females are aggressive in the non-breeding season and (2). whether DHEA is detectable in the plasma at that time. We conducted simulated territorial intrusions (STIs) with live decoys to male and female free-living spotted antbirds in central Panama. Non-breeding males and females displayed robust aggressive responses to STIs, and responded more intensely to decoys of their own sex. In both sexes, plasma DHEA concentrations were detectable and higher than levels of testosterone (T) and 17beta-estradiol (E(2)). In males, plasma DHEA concentrations were positively correlated with STI duration. Next, we conducted STIs in captive non-breeding birds. Captive males and females displayed robust aggressive behavior. Plasma DHEA concentrations were detectable in both sexes, whereas T was non-detectable (E(2) was not measured). Plasma DHEA concentrations of males were positively correlated with aggressive vocalizations and appeared to increase with longer STI durations. We conclude that male and female spotted antbirds can produce DHEA during the non-breeding season and DHEA may serve as a precursor of sex steroids for the regulation of year-round territorial behavior in both sexes.     

Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes

Zooplanktivory is one of the most distinct trophic niches in coral reef fishes, and a number of skull traits are widely recognized as being adaptations for feeding in midwater on small planktonic prey. Previous studies have concluded that zooplanktivores have larger eyes for sharper visual acuity, reduced mouth structures to match small prey sizes, and longer gill rakers to help retain captured prey. We tested these three traditional hypotheses plus two novel adaptive hypotheses in labrids, a clade of very diverse coral reef fishes that show multiple independent evolutionary origins of zooplanktivory. Using phylogenetic comparative methods with a data set from 21 species, we failed to find larger eyes in three independent transitions to zooplanktivory. Instead, an impression of large eyes may be caused by a size reduction of the anterior facial region. However, two zooplanktivores (Clepticus parrae and Halichoeres pictus) possess several features interpreted as adaptations to zooplankton feeding, namely large lens diameters relative to eye axial length, round pupil shape, and long gill rakers. The third zooplanktivore in our analysis, Cirrhilabrus solorensis, lacks all above features. It remains unclear whether Cirrhilabrus shows optical specializations for capturing planktonic prey. Our results support the prediction that increased visual acuity is adaptive for zooplanktivory, but in labrids increases in eye size are apparently not part of the evolutionary response.     

The origin of modern amphibians: a re‐evaluation

There are currently three competing hypotheses seeking to explain the evolutionary origins of modern amphibians. The lepospondyl hypothesis holds that the lysorophian lepospondyls constitute the sister taxon to all lissamphibians. The temnospondyl hypothesis suggests that modern amphibians are most closely related to the dissorophoid temnospondyls. Finally, the polyphyletic hypothesis posits that the modern amphibian orders have separate evolutionary origins from among different groups of Palaeozoic tetrapods. Here, we review the character matrices used in previous studies. These data sets differ significantly in choice of characters. Therefore, we built a matrix based on data from all three hypotheses and analysed key taxa phylogenetically using both Bayesian inference and parsimony. Uncorrected, the supermatrix yielded inconclusive results, demonstrating the presence of at least two phylogenetic optima. When the data were corrected according to new observations on Doleserpeton, Eocaecilia, and other fossil forms, the phylogeny supported the temnospondyl hypothesis of lissamphibian origins. This conclusion is also supported by a careful study of character changes in the individual lineages. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 457–469.     

Leader preference in Neoconocephalus ensiger katydids: a female preference for a nonheritable male trait

Female preferences for males producing their calls just ahead of their neighbours, leader preferences, are common in acoustically communicating insects and anurans. While these preferences have been well studied, their evolutionary origins remain unclear. We tested whether females gain a fitness benefit by mating with leading males in Neoconocephalus ensiger katydids. We mated leading and following males with random females and measured the number and quality of F₁, the number of F₂ and the heritability of the preferred male trait. We found that females mating with leaders and followers did not differ in the number of F₁ or F₂ offspring. Females mating with leading males had offspring that were in better condition than those mating with following males suggesting a benefit in the form of higher quality offspring. We found no evidence that the male trait, the production of leading calls, was heritable. This suggests that there is no genetic correlate for the production of leading calls and that the fitness benefit gained by females must be a direct benefit, potentially mediated by seminal proteins. The presence of benefits indicates that leader preference is adaptive in N. ensiger, which may explain the evolutionary origin of leader preference; further tests are required to determine whether fitness benefits can explain the phylogenetic distribution of leader preference in Neoconocephalus. The absence of heritability will prevent leader preference from becoming coupled with or exaggerating the male trait and prevent females from gaining a ‘sexy‐sons’ benefit, weakening the overall selection for leader preference.     

Testing eco-evolutionary predictions using fossil data: Phyletic evolution following ecological opportunity*

Fossil sequences provide observations of phenotypes within a lineage over time and represent essential data for increasing our understanding of phyletic evolution beyond microevolutionary timescales. I investigate if fossil time series of the diatom Stephanodiscus niagarae/yellowstonensis follow evolutionary dynamics compatible with hypotheses for how the adaptive landscape changes when a population enters a new environment. The lineage—which has a remarkably detailed stratigraphic record—invaded Yellowstone Lake immediately after recession of ice from the basin 14,000 years ago. Several phyletic models portraying different types of evolutionary dynamics—both compatible and not compatible with changes in the adaptive landscape following ecological opportunity—were fitted to the fossil times-series of S. niagarae/yellowstonensis. Different models best describe the three analyzed traits. Two of the models (a new model of decelerated evolution and an Ornstein–Uhlenbeck model) capture trait dynamics compatible with an event of ecological opportunity, whereas the third model (random walk) does not. Entering a new environment may accordingly affect trait dynamics for thousands of years, but the effects can vary across phenotypes. However, tests of model adequacy reveal shortcomings in all three models explaining the trait dynamics, suggesting model development is needed to more fully understand the phyletic evolution in S. niagarae/yellowstonensis.     

Description and interpretation of adaptive evolution of Escherichia coli K-12 MG1655 by using a genome-scale in silico metabolic model

Genome-scale in silico metabolic networks of Escherichia coli have been reconstructed. By using a constraint-based in silico model of a reconstructed network, the range of phenotypes exhibited by E. coli under different growth conditions can be computed, and optimal growth phenotypes can be predicted. We hypothesized that the end point of adaptive evolution of E. coli could be accurately described a priori by our in silico model since adaptive evolution should lead to an optimal phenotype. Adaptive evolution of E. coli during prolonged exponential growth was performed with M9 minimal medium supplemented with 2 g of alpha-ketoglutarate per liter, 2 g of lactate per liter, or 2 g of pyruvate per liter at both 30 and 37 degrees C, which produced seven distinct strains. The growth rates, substrate uptake rates, oxygen uptake rates, by-product secretion patterns, and growth rates on alternative substrates were measured for each strain as a function of evolutionary time. Three major conclusions were drawn from the experimental results. First, adaptive evolution leads to a phenotype characterized by maximized growth rates that may not correspond to the highest biomass yield. Second, metabolic phenotypes resulting from adaptive evolution can be described and predicted computationally. Third, adaptive evolution on a single substrate leads to changes in growth characteristics on other substrates that could signify parallel or opposing growth objectives. Together, the results show that genome-scale in silico metabolic models can describe the end point of adaptive evolution a priori and can be used to gain insight into the adaptive evolutionary process for E. coli.     

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage

The evolution of mate choice is a major topic in evolutionary biology because it is thought to be a key factor in trait and species diversification. Here, we aim at uncovering the ecological conditions and genetic architecture enabling the puzzling evolution of disassortative mating based on adaptive traits. This rare form of mate choice is observed for some polymorphic traits but theoretical predictions on the emergence and persistence of this behavior are largely lacking. Thus, we developed a mathematical model to specifically understand the evolution of disassortative mating based on mimetic color pattern in the polymorphic butterfly Heliconius numata. We confirm that heterozygote advantage favors the evolution of disassortative mating and show that disassortative mating is more likely to emerge if at least one allele at the trait locus is free from any recessive deleterious mutations. We modeled different possible genetic architectures underlying mate choice behavior, such as self‐referencing alleles, or specific preference or rejection alleles. Our results showed that self‐referencing or rejection alleles linked to the color pattern locus enable the emergence of disassortative mating. However, rejection alleles allow the emergence of disassortative mating only when the color pattern and preference loci are tightly linked.     

The evolution of religious belief in humans: a brief review with a focus on cognition

Religion has been a widely present feature of human beings. This review explores developments in the evolutionary cognitive psychology of religion and provides critical evaluation of the different theoretical positions. Generally scholars have either believed religion is adaptive, a by-product of adaptive psychological features or maladaptive and varying amounts of empirical evidence supports each position. The adaptive position has generated the costly signalling theory of religious ritual and the group selection theory. The by-product position has identified psychological machinery that has been co-opted by religion. The maladaptive position has generated the meme theory of religion. The review concludes that the by-product camp enjoys the most support in the scientific community and suggests ways forward for an evolutionarily significant study of religion.     

Adaptations and history

The historical definition of adaptations has come into wide use as comparative biologists have applied methods of phylogenetic analysis to a variety of evolutionary problems. Here we point out a number of difficulties in applying historical methods to the study of adaptation, especially in cases where a trait has arisen but once. In particular, the potential complexity of the genetic correlations among phenotypic traits, performance variables and fitness makes inferring past patterns of selection from comparative data difficult. A given pattern of character distribution may support many alternative hypotheses of mechanism. While phylogenetic data are limited in their ability to reveal evolutionary mechanisms, they have always been an important source of adaptive hypotheses and will continue to be so.     

The evolution of inequality

Understanding how systems of political and economic inequality evolved from relatively egalitarian origins has long been a focus of anthropological inquiry. Many hypotheses have been suggested to link socio‐ecological features with the rise and spread of inequality, and empirical tests of these hypotheses in prehistoric and extant societies are increasing. In this review, we synthesize several streams of theory relevant to understanding the evolutionary origins, spread, and adaptive significance of inequality. We argue that while inequality may be produced by a variety of localized processes, its evolution is fundamentally dependent on the economic defensibility and transmissibility of wealth. Furthermore, these properties of wealth could become persistent drivers of inequality only following a shift to a more stable climate in the Holocene. We conclude by noting several key areas for future empirical research, emphasizing the need for more analyses of contemporary shifts toward institutionalized inequality as well as prehistoric cases.