Adaptive evolution in the human genome

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Adaptive evolution results from the propagation of advantageous mutations through positive selection. This is the modern synthesis of the process which Darwin and Wallace originally identified as the mechanism of evolution. However, in the last half century there has been considerable debate as to whether evolutionary changes at the molecular level are largely driven by natural selection or random genetic drift. Unsurprisingly, the forces which drive evolutionary changes in our own species’ lineage have been of particular interest. Quantifying adaptive evolution in the human genome gives insights into our own evolutionary history and helps to resolve this neutralist-selectionist debate. Identifying specific regions of the human genome that show evidence of adaptive evolution helps us find functionally significant genes, including genes important for human health, such as those associated with diseases.

Methods

The methods used to identify adaptive evolution are generally devised to test the null hypothesis of neutral evolution, which, if rejected, provides evidence of adaptive evolution. These tests can be broadly divided into two categories.

Firstly, there are methods that use a comparative approach to search for evidence of function altering mutations. The dN/dS rates-ratio test estimates ω, the rates at which nonsynonymous ('dN') and synonymous ('dS') nucleotide substitutions occur ('synonymous' nucleotide substitutions do not lead to a change in the coding amino acid, while 'nonsynonymous' ones do). In this model, neutral evolution is considered the null hypothesis, in which dN and dS approximately balance so that ω ≈ 1. The two alternative hypotheses are a relative absence of nonsynonymous substitutions (dN < dS; ω < 1), suggesting the effect on fitness ('fitness effect', or 'selection pressure') of such mutations is negative (purifying selection has operated over time); or a relative excess of nonsynonymous substitutions (dN > dS; ω > 1), indicating positive effect on fitness, i.e. diversifying selection (Yang and Bielawski 2000).

The McDonald-Kreitman (MK) test quantifies the amount of adaptive evolution occurring by estimating the proportion of nonsynonymous substitutions which are adaptive, referred to as α (McDonald and Kreitman 1991, Eyre-Walker 2006). α is calculated as: α = 1-(dspn/dnps), where dn and ds are as above, and pn and ps are the number of nonsynonymous (fitness effect assumed neutral or deleterious) and synonymous (fitness effect assumed neutral) polymorphisms respectively (Eyre-Walker 2006).

Note, both these tests are presented here in basic forms, and these tests are normally modified considerably to account for other factors, such as the effect of slightly deleterious mutations.

The other methods for detecting adaptive evolution use genome wide approaches, often to look for evidence of selective sweeps. Evidence of complete selective sweeps is shown by a decrease in genetic diversity, and can be inferred from comparing the patterns of the Site Frequency Spectrum (SFS, i.e. the allele frequency distribution) obtained with the SFS expected under a neutral model (Willamson et al. 2007). Partial selective sweeps provide evidence of the most recent adaptive evolution, and the methods identify adaptive evolution by searching for regions with a high proportion of derived alleles (Sabeti et al. 2006).

Examining patterns of Linkage Disequilibrium (LD) can locate signatures of adaptive evolution (Hawks et al. 2007, Voight et al. 2006). LD tests work on the basic principle that, assuming equal recombination rates, LD will rise with increasing natural selection. These genomic methods can also be applied to search for adaptive evolution in non-coding DNA, where putatively neutral sites are hard to identify (Ponting and Lunter 2006).

Another recent method used to detect selection in non-coding sequences examines insertions and deletions (indels), rather than point mutations (Lunter et al. 2006), although the method has only been applied to examine patterns of negative selection.

Amount of adaptive evolution

Coding DNA

Many different studies have attempted to quantify the amount of adaptive evolution in the human genome, the vast majority using the comparative approaches outlined above. Although there are discrepancies between studies, generally there is relatively little evidence of adaptive evolution in protein coding DNA, with estimates of adaptive evolution often near 0% (see Table 1). The most obvious exception to this is the 35% estimate of α (Fay et al. 2001). This comparatively early study used relatively few loci (fewer than 200) for their estimate, and the polymorphism and divergence data used was obtained from different genes, both of which may have led to an overestimate of α. The next highest estimate is the 20% value of α (Zhang and Li 2005). However, the MK test used in this study was sufficiently weak that the authors state that this value of α is not statistically significantly different from 0%. Nielsen et al. (2005a)’s estimate that 9.8% of genes have undergone adaptive evolution also has a large margin of error associated with it, and their estimate shrinks dramatically to 0.4% when they stipulate that the degree of certainty that there has been adaptive evolution must be 95% or more.

This raises an important issue, which is that many of these tests for adaptive evolution are very weak. Therefore, the fact that many estimates are at (or very near to) 0% does not rule out the occurrence of any adaptive evolution in the human genome, but simply shows that positive selection is not frequent enough to be detected by the tests. In fact, the most recent study mentioned states that confounding variables, such as demographic changes, mean that the true value of α may be as high as 40% (Eyre-Walker and Keightley 2009). Another recent study, which uses a relatively robust methodology, estimates α at 10-20% Boyko et al. (2008). Clearly, the debate over the amount of adaptive evolution occurring in human coding DNA is not yet resolved.

Even if low estimates of α are accurate, a small proportion of substitutions evolving adaptively can still equate to a considerable amount of coding DNA. Many authors, whose studies have small estimates of the amount of adaptive evolution in coding DNA, nevertheless accept that there has been some adaptive evolution in this DNA, because these studies identify specific regions within the human genome which have been evolving adaptively (e.g. Bakewell et al. (2007)). More genes underwent positive selection in chimpanzee evolution than in human.

The generally low estimates of adaptive evolution in human coding DNA can be contrasted with other species. Bakewell et al. (2007) found more evidence of adaptive evolution in chimpanzees than humans, with 1.7% of chimpanzee genes showing evidence of adaptive evolution (compared with the 1.1% estimate for humans; see Table 1). Comparing humans with more distantly related animals, an early estimate for α in Drosophila species was 45% (Smith and Eyre-Walker 2002), and later estimates largely agree with this (Eyre-Walker 2006). Bacteria and viruses generally show even more evidence of adaptive evolution; research shows values of α in a range of 50-85%, depending on the species examined (Eyre-Walker 2006). Generally, there does appear to be a positive correlation between (effective) population size of the species, and amount of adaptive evolution occurring in the coding DNA regions. This may be because random genetic drift becomes less powerful at altering allele frequencies, compared to natural selection, as population size increases.

Non-coding DNA

Estimates of the amount of adaptive evolution in non-coding DNA are generally very low, although fewer studies have been done on non-coding DNA. As with the coding DNA however, the methods currently used are relatively weak. Ponting and Lunter (2006) speculate that underestimates may be even more severe in non-coding DNA, because non-coding DNA may undergo periods of functionality (and adaptive evolution), followed by periods of neutrality. If this is true, current methods for detecting adaptive evolution are inadequate to account for such patterns. Additionally, even if low estimates of the amount of adaptive evolution are correct, this can still equate to a large amount of adaptively evolving non-coding DNA, since non-coding DNA makes up approximately 98% of the DNA in the human genome. For example, Ponting and Lunter (2006) detect a modest 0.03% of non-coding DNA showing evidence of adaptive evolution, but this still equates to approximately 1 Mb of adaptively evolving DNA. Where there is evidence of adaptive evolution (which implies functionality) in non-coding DNA, these regions are generally thought to be involved in the regulation of protein coding sequences.

As with humans, fewer studies have searched for adaptive evolution in non-coding regions of other organisms. However, where research has been done on Drosophila, there appears to be large amounts of adaptively evolving non-coding DNA. Andolfatto (2005) estimated that adaptive evolution has occurred in 60% of untranslated mature portions of mRNAs, and in 20% of intronic and intergenic regions. If this is true, this would imply that much non-coding DNA could be of more functional importance than coding DNA, dramatically altering the consensus view. However, this would still leave unanswered what function all this non-coding DNA performs, as the regulatory activity observed thus far is in just a tiny proportion of the total amount of non-coding DNA. Ultimately, significantly more evidence needs to be gathered to substantiate this viewpoint.

Variation between human populations

Several recent studies have compared the amounts of adaptive evolution occurring between different populations within the human species. Williamson et al. (2007) found more evidence of adaptive evolution in European and Asian populations than African American populations. Assuming African Americans are representative of Africans, these results makes sense intuitively, because humans spread out of Africa approximately 50,000 years ago (according to the consensus Out-of-Africa hypothesis of human origins (Klein 2009)), and these humans would have adapted to the new environments they encountered. By contrast, African populations remained in a similar environment for the following tens of thousands of years, and were therefore probably nearer their adaptive peak for the environment. However, Voight et al. (2006) found evidence of more adaptive evolution in Africans, than in Non-Africans (East Asian and European populations examined), and Boyko et al. (2008) found no significant difference in the amount of adaptive evolution occurring between different human populations. Therefore, the evidence obtained so far is inconclusive as to what extent different human populations have undergone different amounts of adaptive evolution.

Rate of adaptive evolution

The rate of adaptive evolution in the human genome has often been assumed to be constant over time. For example, the 35% estimate for α calculated by Fay et al. (2001) led them to conclude that there was one adaptive substitution in the human lineage every 200 years since human divergence from old-world monkeys. However, even if the original value of α is accurate for a particular time period, this extrapolation is still invalid. This is because there has been a large acceleration in the amount of positive selection in the human lineage over the last 40,000 years, in terms of the number of genes that have undergone adaptive evolution (Hawks et al. 2007). This agrees with simple theoretical predictions, because the human population size has expanded dramatically in the last 40,000 years, and with more people, there should be more adaptive substitutions. Hawks et al. (2007) argue that demographic changes (particularly population expansion) may greatly facilitate adaptive evolution, an argument that somewhat corroborates the positive correlation inferred between population size and amount of adaptive evolution occurring mentioned previously.

It has been suggested that cultural evolution may have replaced genetic evolution, and hence slowed the rate of adaptive evolution over the past 10,000 years. However, it is possible that cultural evolution could actually increase genetic adaption. Cultural evolution has vastly increased communication and contact between different populations, and this provides much greater opportunities for genetic admixture between the different populations (Hawks et al. 2007). However, recent cultural phenomena, such as modern medicine and the smaller variation in modern family sizes, may reduce genetic adaption as natural selection is relaxed, overriding the increased potential for adaptation due to greater genetic admixture.

Strength of positive selection

Studies generally do not attempt to quantify the average strength of selection propagating advantageous mutations in the human genome. Many models make assumptions about how strong selection is, and some of the discrepancies between the estimates of the amounts of adaptive evolution occurring have been attributed to the use of such differing assumptions (Eyre-Walker 2006). The way to accurately estimate the average strength of positive selection acting on the human genome is by inferring the distribution of fitness effects (DFE) of new advantageous mutations in the human genome, but this DFE is difficult to infer because new advantageous mutations are very rare (Boyko et al. 2008). The DFE may be exponential shaped in an adapted population (Eyre-Walker and Keightley 2007). However, more research is required to produce more accurate estimates of the average strength of positive selection in humans, which will in turn improve the estimates of the amount of adaptive evolution occurring in the human genome (Boyko et al. 2008).

Regions of the genome which show evidence of adaptive evolution

A considerable number of studies have used genomic methods to identify specific human genes that show evidence of adaptive evolution. Table 2 gives selected examples of such genes for each gene type discussed, but provides nowhere near an exhaustive list of the human genes showing evidence of adaptive evolution. Below are listed some of the types of gene which show strong evidence of adaptive evolution in the human genome.

• Disease genes

Bakewell et al. (2007) found that a relatively large proportion (9.7%) of positively selected genes were associated with diseases. This may be because diseases can be adaptive in some contexts. For example, schizophrenia has been linked with increased creativity (Crespi et al. 2007), perhaps a useful trait for obtaining food or attracting mates in Palaeolithic times. Alternatively, the adaptive mutations may be the ones which reduce the chance of disease arising due to other mutations. However, this second explanation seems unlikely, because the mutation rate in the human genome is fairly low, so selection would be relatively weak.

• Immune genes

417 genes involved in the immune system showed strong evidence of adaptive evolution in the study of Nielsen et al. (2005a). This is probably because the immune genes may become involved in an evolutionary arms race with bacteria and viruses (Daugherty and Malik 2012; Van der Lee et al. 2017). These pathogens evolve very rapidly, so selection pressures change quickly, giving more opportunity for adaptive evolution.

• Testes genes

247 genes in the testes showed evidence of adaptive evolution in the study of Nielsen et al. (2005a). This could be partially due to sexual antagonism. Male-female competition could facilitate an arms race of adaptive evolution. However, in this situation you would expect to find evidence of adaptive evolution in the female sexual organs also, but there is less evidence of this. Sperm competition is another possible explanation. Sperm competition is strong, and sperm can improve their chances of fertilising the female egg in a variety of ways, including increasing their speed, stamina or response to chemoattractants (Swanson and Vacquier 2002).

• Olfactory genes

Genes involved in detecting smell show strong evidence of adaptive evolution (Voight et al. 2006), probably due to the fact that the smells encountered by humans have changed recently in their evolutionary history (Williamson et al. 2007). Humans’ sense of smell has played an important role in determining the safety of food sources.

• Nutrition genes

Genes involved in lactose metabolism show particularly strong evidence of adaptive evolution amongst the genes involved in nutrition. A mutation linked to lactase persistence shows very strong evidence of adaptive evolution in European and American populations (Williamson et al. 2007), populations where pastoral farming for milk has been historically important.

• Pigmentation genes

Pigmentation genes show particularly strong evidence of adaptive evolution in non-African populations (Williamson et al. 2007). This is likely to be because those humans that left Africa approximately 50,000 years ago, entered less sunny climates, and so were under new selection pressures to obtain enough Vitamin D from the weakened sunlight.

• Brain genes?

There is some evidence of adaptive evolution in genes linked to brain development, but some of these genes are often associated with diseases, e.g. microcephaly (see Table 2). However, there is a particular interest in the search for adaptive evolution in brain genes, despite the ethical issues surrounding such research. If more adaptive evolution was discovered in brain genes in one human population than another, then this information could be interpreted as showing greater intelligence in the more adaptively evolved population.

• Other

Other gene types showing considerable evidence of adaptive evolution (but generally less evidence than the types discussed) include: genes on the X chromosome, nervous system genes, genes involved in apoptosis, genes coding for skeletal traits, and possibly genes associated with speech (Nielsen et al. 2005a, Williamson et al. 2007, Voight et al. 2006, Krause et al. 2007).

Difficulties in identifying positive selection

As noted previously, many of the tests used to detect adaptive evolution have very large degrees of uncertainty surrounding their estimates. While there are many different modifications applied to individual tests to overcome the associated problems, two types of confounding variables are particularly important in hindering the accurate detection of adaptive evolution: demographic changes and biased gene conversion.

Demographic changes are particularly problematic and may severely bias estimates of adaptive evolution. The human lineage has undergone both rapid population size contractions and expansions over its evolutionary history, and these events will change many of the signatures thought to be characteristic of adaptive evolution (Nielsen et al. 2007). Some genomic methods have been shown through simulations to be relatively robust to demographic changes (e.g. Willamson et al. 2007). However, no tests are completely robust to demographic changes, and new genetic phenomena linked to demographic changes have recently been discovered. This includes the concept of “surfing mutations”, where new mutations can be propagated with a population expansion (Klopfstein et al. 2006).

A phenomenon which could severely alter the way we look for signatures of adaptive evolution is biased gene conversion (BGC) (Galtier and Duret 2007). Meiotic recombination between homologous chromosomes that are heterozygous at a particular locus can produce a DNA mismatch. DNA repair mechanisms are biased towards repairing a mismatch to the CG base pair. This will lead allele frequencies to change, leaving a signature of non-neutral evolution (Galtier et al. 2001). The excess of AT to GC mutations in human genomic regions with high substitution rates (human accelerated regions, HARs) implies that BGC has occurred frequently in the human genome (Pollard et al. 2006, Galtier and Duret 2007). Initially, it was postulated that BGC could have been adaptive (Galtier et al. 2001), but more recent observations have made this seem unlikely. Firstly, some HARs show no substantial signs of selective sweeps around them. Secondly, HARs tend to be present in regions with high recombination rates (Pollard et al. 2006). In fact, BGC could lead to HARs containing a high frequency of deleterious mutations (Galtier and Duret 2007). However, it is unlikely that HARs are generally maladaptive, because DNA repair mechanisms themselves would be subject to strong selection if they propagated deleterious mutations. Either way, BGC should be further investigated, because it may force radical alteration of the methods which test for the presence of adaptive evolution.

Adaptation

In biology, adaptation has three related meanings. Firstly, it is the dynamic evolutionary process that fits organisms to their environment, enhancing their evolutionary fitness. Secondly, it is a state reached by the population during that process. Thirdly, it is a phenotypic trait or adaptive trait, with a functional role in each individual organism, that is maintained and has evolved through natural selection.

Historically, adaptation has been described from the time of the ancient Greek philosophers such as Empedocles and Aristotle. In 18th and 19th century natural theology, adaptation was taken as evidence for the existence of a deity. Charles Darwin proposed instead that it was explained by natural selection.

Adaptation is related to biological fitness, which governs the rate of evolution as measured by change in gene frequencies. Often, two or more species co-adapt and co-evolve as they develop adaptations that interlock with those of the other species, such as with flowering plants and pollinating insects. In mimicry, species evolve to resemble other species; in Müllerian mimicry this is a mutually beneficial co-evolution as each of a group of strongly defended species (such as wasps able to sting) come to advertise their defences in the same way. Features evolved for one purpose may be co-opted for a different one, as when the insulating feathers of dinosaurs were co-opted for bird flight.

Adaptation is a major topic in the philosophy of biology, as it concerns function and purpose (teleology). Some biologists try to avoid terms which imply purpose in adaptation, not least because it suggests a deity's intentions, but others note that adaptation is necessarily purposeful.

History

Adaptation is an observable fact of life accepted by philosophers and natural historians from ancient times, independently of their views on evolution, but their explanations differed. Empedocles did not believe that adaptation required a final cause (a purpose), but thought that it "came about naturally, since such things survived." Aristotle did believe in final causes, but assumed that species were fixed.

The second of Jean-Baptiste Lamarck's two factors (the first being a complexifying force) was an adaptive force that causes animals with a given body plan to adapt to circumstances by inheritance of acquired characteristics, creating a diversity of species and genera.

In natural theology, adaptation was interpreted as the work of a deity and as evidence for the existence of God. William Paley believed that organisms were perfectly adapted to the lives they led, an argument that shadowed Gottfried Wilhelm Leibniz, who had argued that God had brought about "the best of all possible worlds." Voltaire's satire Dr. Pangloss is a parody of this optimistic idea, and David Hume also argued against design. The Bridgewater Treatises are a product of natural theology, though some of the authors managed to present their work in a fairly neutral manner. The series was lampooned by Robert Knox, who held quasi-evolutionary views, as the Bilgewater Treatises. Charles Darwin broke with the tradition by emphasising the flaws and limitations which occurred in the animal and plant worlds.

Jean-Baptiste Lamarck proposed a tendency for organisms to become more complex, moving up a ladder of progress, plus "the influence of circumstances," usually expressed as use and disuse. This second, subsidiary element of his theory is what is now called Lamarckism, a proto-evolutionary hypothesis of the inheritance of acquired characteristics, intended to explain adaptations by natural means.

Other natural historians, such as Buffon, accepted adaptation, and some also accepted evolution, without voicing their opinions as to the mechanism. This illustrates the real merit of Darwin and Alfred Russel Wallace, and secondary figures such as Henry Walter Bates, for putting forward a mechanism whose significance had only been glimpsed previously. A century later, experimental field studies and breeding experiments by people such as E. B. Ford and Theodosius Dobzhansky produced evidence that natural selection was not only the 'engine' behind adaptation, but was a much stronger force than had previously been thought.

General principles

The significance of an adaptation can only be understood in relation to the total biology of the species.

— Julian Huxley, Evolution: The Modern Synthesis

What adaptation is

Adaptation is primarily a process rather than a physical form or part of a body. An internal parasite (such as a liver fluke) can illustrate the distinction: such a parasite may have a very simple bodily structure, but nevertheless the organism is highly adapted to its specific environment. From this we see that adaptation is not just a matter of visible traits: in such parasites critical adaptations take place in the life cycle, which is often quite complex. However, as a practical term, "adaptation" often refers to a product: those features of a species which result from the process. Many aspects of an animal or plant can be correctly called adaptations, though there are always some features whose function remains in doubt. By using the term adaptation for the evolutionary process, and adaptive trait for the bodily part or function (the product), one may distinguish the two different senses of the word.

Adaptation is one of the two main processes that explain the observed diversity of species, such as the different species of Darwin's finches. The other process is speciation, in which new species arise, typically through reproductive isolation. An example widely used today to study the interplay of adaptation and speciation is the evolution of cichlid fish in African lakes, where the question of reproductive isolation is complex.

Adaptation is not always a simple matter where the ideal phenotype evolves for a given environment. An organism must be viable at all stages of its development and at all stages of its evolution. This places constraints on the evolution of development, behaviour, and structure of organisms. The main constraint, over which there has been much debate, is the requirement that each genetic and phenotypic change during evolution should be relatively small, because developmental systems are so complex and interlinked. However, it is not clear what "relatively small" should mean, for example polyploidy in plants is a reasonably common large genetic change. The origin of eukaryotic endosymbiosis is a more dramatic example.

All adaptations help organisms survive in their ecological niches. The adaptive traits may be structural, behavioural or physiological. Structural adaptations are physical features of an organism, such as shape, body covering, armament, and internal organization. Behavioural adaptations are inherited systems of behaviour, whether inherited in detail as instincts, or as a neuropsychological capacity for learning. Examples include searching for food, mating, and vocalizations. Physiological adaptations permit the organism to perform special functions such as making venom, secreting slime, and phototropism), but also involve more general functions such as growth and development, temperature regulation, ionic balance and other aspects of homeostasis. Adaptation affects all aspects of the life of an organism.

The following definitions are given by the evolutionary biologist Theodosius Dobzhansky:

1. Adaptation is the evolutionary process whereby an organism becomes better able to live in its habitat or habitats.

2. Adaptedness is the state of being adapted: the degree to which an organism is able to live and reproduce in a given set of habitats.

3. An adaptive trait is an aspect of the developmental pattern of the organism which enables or enhances the probability of that organism surviving and reproducing.

What adaptation is not

Some generalists, such as birds, have the flexibility to adapt to urban areas.

Adaptation differs from flexibility, acclimatization, and learning, all of which are changes during life which are not inherited. Flexibility deals with the relative capacity of an organism to maintain itself in different habitats: its degree of specialization. Acclimatization describes automatic physiological adjustments during life; learning means improvement in behavioural performance during life.

Flexibility stems from phenotypic plasticity, the ability of an organism with a given genotype (genetic type) to change its phenotype (observable characteristics) in response to changes in its habitat, or to move to a different habitat. The degree of flexibility is inherited, and varies between individuals. A highly specialized animal or plant lives only in a well-defined habitat, eats a specific type of food, and cannot survive if its needs are not met. Many herbivores are like this; extreme examples are koalas which depend on Eucalyptus, and giant pandas which require bamboo. A generalist, on the other hand, eats a range of food, and can survive in many different conditions. Examples are humans, rats, crabs and many carnivores. The tendency to behave in a specialized or exploratory manner is inherited—it is an adaptation. Rather different is developmental flexibility: "An animal or plant is developmentally flexible if when it is raised in or transferred to new conditions, it changes in structure so that it is better fitted to survive in the new environment," writes evolutionary biologist John Maynard Smith.

If humans move to a higher altitude, respiration and physical exertion become a problem, but after spending time in high altitude conditions they acclimatize to the reduced partial pressure of oxygen, such as by producing more red blood cells. The ability to acclimatize is an adaptation, but the acclimatization itself is not. The reproductive rate declines, but deaths from some tropical diseases also go down. Over a longer period of time, some people are better able to reproduce at high altitudes than others. They contribute more heavily to later generations, and gradually by natural selection the whole population becomes adapted to the new conditions. This has demonstrably occurred, as the observed performance of long-term communities at higher altitude is significantly better than the performance of new arrivals, even when the new arrivals have had time to acclimatize.

Adaptedness and fitness

There is a relationship between adaptedness and the concept of fitness used in population genetics. Differences in fitness between genotypes predict the rate of evolution by natural selection. Natural selection changes the relative frequencies of alternative phenotypes, insofar as they are heritable. However, a phenotype with high adaptedness may not have high fitness. Dobzhansky mentioned the example of the Californian redwood, which is highly adapted, but a relict species in danger of extinction. Elliott Sober commented that adaptation was a retrospective concept since it implied something about the history of a trait, whereas fitness predicts a trait's future.

1. Relative fitness. The average contribution to the next generation by a genotype or a class of genotypes, relative to the contributions of other genotypes in the population. This is also known as Darwinian fitness, selection coefficient, and other terms.

2. Absolute fitness. The absolute contribution to the next generation by a genotype or a class of genotypes. Also known as the Malthusian parameter when applied to the population as a whole.

3. Adaptedness. The extent to which a phenotype fits its local ecological niche. Researchers can sometimes test this through a reciprocal transplant.

In this sketch of a fitness landscape, a population can evolve by following the arrows to the adaptive peak at point B, and the points A and C are local optima where a population could become trapped.

Sewall Wright proposed that populations occupy adaptive peaks on a fitness landscape. To evolve to another, higher peak, a population would first have to pass through a valley of maladaptive intermediate stages, and might be "trapped" on a peak that is not optimally adapted.

Types

Adaptation is the heart and soul of evolution.

— Niles Eldredge, Reinventing Darwin: The Great Debate at the High Table of Evolutionary Theory

Changes in habitat

Before Darwin, adaptation was seen as a fixed relationship between an organism and its habitat. It was not appreciated that as the climate changed, so did the habitat; and as the habitat changed, so did the biota. Also, habitats are subject to changes in their biota: for example, invasions of species from other areas. The relative numbers of species in a given habitat are always changing. Change is the rule, though much depends on the speed and degree of the change. When the habitat changes, three main things may happen to a resident population: habitat tracking, genetic change or extinction. In fact, all three things may occur in sequence. Of these three effects only genetic change brings about adaptation. When a habitat changes, the resident population typically moves to more suitable places; this is the typical response of flying insects or oceanic organisms, which have wide (though not unlimited) opportunity for movement. This common response is called habitat tracking. It is one explanation put forward for the periods of apparent stasis in the fossil record (the punctuated equilibrium theory).

Genetic change

Genetic change occurs in a population when natural selection and mutations act on its genetic variability. The first pathways of enzyme-based metabolism may have been parts of purine nucleotide metabolism, with previous metabolic pathways being part of the ancient RNA world. By this means, the population adapts genetically to its circumstances. Genetic changes may result in visible structures, or may adjust physiological activity in a way that suits the habitat. The varying shapes of the beaks of Darwin's finches, for example, are driven by differences in the ALX1 gene.

Habitats and biota do frequently change. Therefore, it follows that the process of adaptation is never finally complete. Over time, it may happen that the environment changes little, and the species comes to fit its surroundings better and better. On the other hand, it may happen that changes in the environment occur relatively rapidly, and then the species becomes less and less well adapted. Seen like this, adaptation is a genetic tracking process, which goes on all the time to some extent, but especially when the population cannot or does not move to another, less hostile area. Given enough genetic change, as well as specific demographic conditions, an adaptation may be enough to bring a population back from the brink of extinction in a process called evolutionary rescue. Adaptation does affect, to some extent, every species in a particular ecosystem.

Leigh Van Valen thought that even in a stable environment, competing species constantly had to adapt to maintain their relative standing. This became known as the Red Queen hypothesis, as seen in host-parasite interaction.

Existing genetic variation and mutation were the traditional sources of material on which natural selection could act. In addition, horizontal gene transfer is possible between organisms in different species, using mechanisms as varied as gene cassettes, plasmids, transposons and viruses such as bacteriophages.

Co-adaptation

Pollinating insects are co-adapted with flowering plants.

In coevolution, where the existence of one species is tightly bound up with the life of another species, new or 'improved' adaptations which occur in one species are often followed by the appearance and spread of corresponding features in the other species. These co-adaptational relationships are intrinsically dynamic, and may continue on a trajectory for millions of years, as has occurred in the relationship between flowering plants and pollinating insects.

Mimicry

Images A and B show real wasps; the others show Batesian mimics: three hoverflies and one beetle.

Bates' work on Amazonian butterflies led him to develop the first scientific account of mimicry, especially the kind of mimicry which bears his name: Batesian mimicry. This is the mimicry by a palatable species of an unpalatable or noxious species (the model), gaining a selective advantage as predators avoid the model and therefore also the mimic. Mimicry is thus an anti-predator adaptation. A common example seen in temperate gardens is the hoverfly, many of which—though bearing no sting—mimic the warning coloration of hymenoptera (wasps and bees). Such mimicry does not need to be perfect to improve the survival of the palatable species.

Bates, Wallace and Fritz Müller believed that Batesian and Müllerian mimicry provided evidence for the action of natural selection, a view which is now standard amongst biologists.

Trade-offs

It is a profound truth that Nature does not know best; that genetical evolution... is a story of waste, makeshift, compromise and blunder.

— Peter Medawar, The Future of Man

All adaptations have a downside: horse legs are great for running on grass, but they can't scratch their backs; mammals' hair helps temperature, but offers a niche for ectoparasites; the only flying penguins do is under water. Adaptations serving different functions may be mutually destructive. Compromise and makeshift occur widely, not perfection. Selection pressures pull in different directions, and the adaptation that results is some kind of compromise.

Since the phenotype as a whole is the target of selection, it is impossible to improve simultaneously all aspects of the phenotype to the same degree.

— Ernst Mayr, The Growth of Biological Thought: Diversity, Evolution, and Inheritance

Consider the antlers of the Irish elk, (often supposed to be far too large; in deer antler size has an allometric relationship to body size). Obviously, antlers serve positively for defence against predators, and to score victories in the annual rut. But they are costly in terms of resource. Their size during the last glacial period presumably depended on the relative gain and loss of reproductive capacity in the population of elks during that time. As another example, camouflage to avoid detection is destroyed when vivid coloration is displayed at mating time. Here the risk to life is counterbalanced by the necessity for reproduction.

Stream-dwelling salamanders, such as Caucasian salamander or Gold-striped salamander have very slender, long bodies, perfectly adapted to life at the banks of fast small rivers and mountain brooks. Elongated body protects their larvae from being washed out by current. However, elongated body increases risk of desiccation and decreases dispersal ability of the salamanders; it also negatively affects their fecundity. As a result, fire salamander, less perfectly adapted to the mountain brook habitats, is in general more successful, have a higher fecundity and broader geographic range.

An Indian peacock's train
in full display

The peacock's ornamental train (grown anew in time for each mating season) is a famous adaptation. It must reduce his maneuverability and flight, and is hugely conspicuous; also, its growth costs food resources. Darwin's explanation of its advantage was in terms of sexual selection: "This depends on the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction." The kind of sexual selection represented by the peacock is called 'mate choice,' with an implication that the process selects the more fit over the less fit, and so has survival value. The recognition of sexual selection was for a long time in abeyance, but has been rehabilitated.

The conflict between the size of the human foetal brain at birth, (which cannot be larger than about 400 cm³, else it will not get through the mother's pelvis) and the size needed for an adult brain (about 1400 cm³), means the brain of a newborn child is quite immature. The most vital things in human life (locomotion, speech) just have to wait while the brain grows and matures. That is the result of the birth compromise. Much of the problem comes from our upright bipedal stance, without which our pelvis could be shaped more suitably for birth. Neanderthals had a similar problem.

As another example, the long neck of a giraffe brings benefits but at a cost. The neck of a giraffe can be up to 2 m (6 ft 7 in) in length. The benefits are that it can be used for inter-species competition or for foraging on tall trees where shorter herbivores cannot reach. The cost is that a long neck is heavy and adds to the animal's body mass, requiring additional energy to build the neck and to carry its weight around.

Shifts in function

Adaptation and function are two aspects of one problem

— Julian Huxley, Evolution: The Modern Synthesis

Pre-adaptation

Pre-adaptation occurs when a population has characteristics which by chance are suited for a set of conditions not previously experienced. For example, the polyploid cordgrass Spartina townsendii is better adapted than either of its parent species to their own habitat of saline marsh and mud-flats. Among domestic animals, the White Leghorn chicken is markedly more resistant to vitamin B₁ deficiency than other breeds; on a plentiful diet this makes no difference, but on a restricted diet this preadaptation could be decisive.

Pre-adaptation may arise because a natural population carries a huge quantity of genetic variability. In diploid eukaryotes, this is a consequence of the system of sexual reproduction, where mutant alleles get partially shielded, for example, by genetic dominance. Microorganisms, with their huge populations, also carry a great deal of genetic variability. The first experimental evidence of the pre-adaptive nature of genetic variants in microorganisms was provided by Salvador Luria and Max Delbrück who developed the Fluctuation Test, a method to show the random fluctuation of pre-existing genetic changes that conferred resistance to bacteriophages in Escherichia coli.

Co-option of existing traits: exaptation

The feathers of Sinosauropteryx, a dinosaur with feathers, were used for insulation, making them an exaptation for flight.

Features that now appear as adaptations sometimes arose by co-option of existing traits, evolved for some other purpose. The classic example is the ear ossicles of mammals, which we know from paleontological and embryological evidence originated in the upper and lower jaws and the hyoid bone of their synapsid ancestors, and further back still were part of the gill arches of early fish. The word exaptation was coined to cover these common evolutionary shifts in function. The flight feathers of birds evolved from the much earlier feathers of dinosaurs, which might have been used for insulation or for display.

Niche construction

Animals including earthworms, beavers and humans use some of their adaptations to modify their surroundings, so as to maximize their chances of surviving and reproducing. Beavers create dams and lodges, changing the ecosystems of the valleys around them. Earthworms, as Darwin noted, improve the topsoil in which they live by incorporating organic matter. Humans have constructed extensive civilizations with cities in environments as varied as the Arctic and hot deserts. In all three cases, the construction and maintenance of ecological niches helps drive the continued selection of the genes of these animals, in an environment that the animals have modified.

Non-adaptive traits

Some traits do not appear to be adaptive as they have a neutral or deleterious effect on fitness in the current environment. Because genes often have pleiotropic effects, not all traits may be functional: they may be what Stephen Jay Gould and Richard Lewontin called spandrels, features brought about by neighbouring adaptations, on the analogy with the often highly decorated triangular areas between pairs of arches in architecture, which began as functionless features.

Another possibility is that a trait may have been adaptive at some point in an organism's evolutionary history, but a change in habitats caused what used to be an adaptation to become unnecessary or even maladapted. Such adaptations are termed vestigial. Many organisms have vestigial organs, which are the remnants of fully functional structures in their ancestors. As a result of changes in lifestyle the organs became redundant, and are either not functional or reduced in functionality. Since any structure represents some kind of cost to the general economy of the body, an advantage may accrue from their elimination once they are not functional. Examples: wisdom teeth in humans; the loss of pigment and functional eyes in cave fauna; the loss of structure in endoparasites.

Extinction and coextinction

If a population cannot move or change sufficiently to preserve its long-term viability, then obviously, it will become extinct, at least in that locale. The species may or may not survive in other locales. Species extinction occurs when the death rate over the entire species exceeds the birth rate for a long enough period for the species to disappear. It was an observation of Van Valen that groups of species tend to have a characteristic and fairly regular rate of extinction.

Just as there is co-adaptation, there is also coextinction, the loss of a species due to the extinction of another with which it is coadapted, as with the extinction of a parasitic insect following the loss of its host, or when a flowering plant loses its pollinator, or when a food chain is disrupted.

Philosophical issues

"Behaviour with a purpose": a young springbok stotting. A biologist might argue that this has the function of signalling to predators, helping the springbok to survive and allowing it to reproduce.

Adaptation raises philosophical issues concerning how biologists speak of function and purpose, as this carries implications of evolutionary history – that a feature evolved by natural selection for a specific reason – and potentially of supernatural intervention – that features and organisms exist because of a deity's conscious intentions. In his biology, Aristotle introduced teleology to describe the adaptedness of organisms, but without accepting the supernatural intention built into Plato's thinking, which Aristotle rejected. Modern biologists continue to face the same difficulty. On the one hand, adaptation is obviously purposeful: natural selection chooses what works and eliminates what does not. On the other hand, biologists by and large reject conscious purpose in evolution. The dilemma gave rise to a famous joke by the evolutionary biologist Haldane: "Teleology is like a mistress to a biologist: he cannot live without her but he's unwilling to be seen with her in public.'" David Hull commented that Haldane's mistress "has become a lawfully wedded wife. Biologists no longer feel obligated to apologize for their use of teleological language; they flaunt it." Ernst Mayr stated that "adaptedness... is a posteriori result rather than an a priori goal-seeking", meaning that the question of whether something is an adaptation can only be determined after the event.

Sexual division of labour

From Wikipedia, the free encyclopedia

https://en.wikipedia.org/wiki/Sexual_division_of_labour 

The sexual division of labour (SDL) is the delegation of different tasks between males and females. Among human foragers, males and females target different types of foods and share them with each other for a mutual or familial benefit. In some species, males and females eat slightly different foods, while in other species, males and females will routinely share food; but only in humans are these two attributes combined. The few remaining hunter-gatherer populations in the world serve as evolutionary models that can help explain the origin of the sexual division of labor. Many studies on the sexual division of labor have been conducted on hunter-gatherer populations, such as the Hadza, a hunter-gatherer population of Tanzania.

Behavioral ecological perspective

Man the hunter vs. woman the gatherer

Both men and women have the option of investing resources either to provision children or to have additional offspring. According to life history theory males and females monitor costs and benefits of each alternative to maximize reproductive fitness; however, trade-off differences do exist between sexes. Females are likely to benefit most from parental care effort because they are certain which offspring are theirs and have relatively few reproductive opportunities, each of which is relatively costly and risky. In contrast, males are less certain of paternity, but may have many more mating opportunities bearing relatively low costs and risks. Though not every hunter-gatherer population pinpoints females to gathering and males to hunting (most notably the Aeta and Ju'/hoansi), the norm of most current populations divide the roles of labor in this manner. Natural selection is more likely to favor male reproductive strategies that stress mating effort and female strategies that emphasize parental investment. As a result, women do the low-risk task of gathering vegetation and underground storage organs that are rich in energy to provide for themselves and offspring. Since women provide a reliable source of caloric intake, men are able to afford a higher risk of failure by hunting animals.

This classic theory of natural selection positing a difference in male and female reproductive strategies has recently been reexamined, with an alternate theory being proposed that promiscuity was encouraged among women and men alike, causing uncertainty among males of the paternity of their offspring, allowing for group cooperation in raising all offspring due to the possibility that any child could be the descendant of a male, similar to observations of the closest relative of humans, the bonobo. Moreover, recent archaeological research done by the anthropologist and archaeologist Steven Kuhn from the University of Arizona suggests that the sexual division of labor did not exist prior to the Upper Paleolithic (50,000 and 10,000 years ago) and developed relatively recently in human history. The sexual division of labor may have arisen to allow humans to acquire food and other resources more efficiently.

Hypotheses for evolutionary origins

Provisioning household

The traditional explanation of the sexual division of labour finds that males and females cooperate within pair bonds by targeting different foods so that everyone in the household benefits. Females may target foods that do not conflict with reproduction and child care, while males will target foods that females do not gather, which increases variance in daily consumption and provides a broader diet for the family. Foraging specialization in particular food groups should increase skill level and thus foraging success rates for targeted foods.

Show-Off / Signaling hypothesis

The "show‐off" hypothesis proposes that men hunt to gain social attention and mating benefits by widely sharing game. This model proposes that hunting functions mainly to provide an honest signal of the underlying genetic quality of hunters, which later yields a mating advantage or social deference. Women tend to target the foods that are most reliable, while men tend to target difficult-to-acquire foods to "signal" their abilities and genetic quality. Hunting is thus viewed as a form of mating or male-male status competition, not familial provisioning. Recent studies on the Hadza have revealed that men hunt mainly to distribute food to their own families rather than sharing with other members of the community. This conclusion suggests evidence against hunting for signaling purposes.

The Victorian Period

The Victorian era has been closely examined by Sally Shuttleworth and company. Women played dual roles and were expected to deliver with conviction in the aspects in which they were required to perform duties in and outside of the household. She states, "Two traditional tropes are here combined: Victorian medical textbooks demonstrated not only woman's biological fitness and adaptation to the sacred role of homemaker, but also her terrifying subjection to the forces of the body. At once angel and demon, woman came to represent both the civilizing power that would cleanse the male from contamination in the brutal world of the economic market and also the rampant, uncontrolled excesses of the material economy."

SDL and optimal foraging theory

Optimal foraging theory (OFT) states that organisms forage in such a way as to maximize their energy intake per unit time. In other words, animals behave in such a way as to find, capture, and consume food containing the most calories while expending the least amount of time possible in doing so. The sexual division of labor provides an appropriate explanation as to why males forgo the opportunity to gather any items with caloric value- a strategy that would seem suboptimal from an energetic standpoint. The OFT suggests that the sexual division of labor is an adaptation that benefits the household; thus, foraging behavior of males will appear optimal at the level of the family. If a hunter-gatherer man does not rely on resources from others and passes up a food item with caloric value, it can be assumed that he is foraging at an optimal level. But, if he passes up the opportunity because it is a food that women routinely gather, then as long as men and women share their spoils, it will be optimal for men to forgo the collection and continue searching for different resources to complement the resources gathered by women.

Cooking and the sexual division of labor

The emergence of cooking in early Homo may have created problems of food theft from women while food was being cooked. As a result, females would recruit male partners to protect them and their resources from others. This concept, known as the theft hypothesis, accommodates an explanation as to why the labor of cooking is strongly associated with the status of women. Women are forced to gather and cook foods because they will not acquire food otherwise and access to resources is critical for their reproductive success. On the contrary, men do not gather because their physical dominance allows them to scrounge cooked foods from women. Thus, women's foraging and food preparation efforts allow men to participate in the high-risk, high-reward activities of hunting. Females, in turn, become increasingly sexually attractive as a means to exploit male interest in investing in her protection.

Evolution of sex differences

Many studies investigating the spatial abilities of men and women have found no significant differences, though metastudies show a male advantage in mental rotation and assessing horizontality and verticality, and a female advantage in spatial memory. The sexual division of labor has been proposed as an explanation for these cognitive differences. Those differences disappear with a short training  or when given a favorable image of woman ability. Furthermore, the individual differences are greater than the average differences, which isn't therefore a valid prediction of a man or woman cognitive ability. This hypothesis argues that males needed the ability to follow prey over long distances and to accurately target their game with projectile technology, and, as a result, male specialization in hunting prowess would have spurred the selection for increased spatial and navigational ability. Similarly, the ability to remember the locations of underground storage organs and other vegetation would have led to an increase in overall efficiency and decrease in total energy expenditure since the time spent searching for food would decrease. Natural selection based on behaviors that increase hunting success and energetic efficiency would bear a positive influence on reproductive success. However, recent research suggests that the sexual division of labor developed relatively recently and that gender roles were not always the same in early-human cultures, contradicting the theory that each sex is naturally predisposed to different types of work.

The discussion of the division of gender roles have been an ongoing debate and Gerda Lerner quotes the philosopher Socrates to demonstrate that the idea of defined gender roles is patriarchal. It also identifies how men and women are capable of performing the same job descriptions with the exception of when it calls for anatomical differences, such as giving birth. "In Book V of the Republic, Plato—in the voice of Socrates—sets down the conditions for the training of the guardians, his elite leadership group. Socrates proposes that women should have the same opportunity as men to be trained as guardians. In support of this he offers a strong statement against making sex differences the basis for discrimination: if the difference [between men and women] consists only in women bearing and men begetting children, this does not amount to proof that a woman differs from a man in respect to the sort of education she should receive; and we shall therefore continue to maintain that our guardians and their wives ought to have the same pursuits.

He continues to add that with the same set of established resources such as education, training and teaching, it creates an atmosphere of equity which helps to further the cause of gender equality. "Socrates proposes the same education for boys and girls, freeing guardian women from housework and child-care. But this female equality of opportunity will serve a larger purpose: the destruction of the family. Plato's aim is to abolish private property, the private family, and with it self-interest in his leadership group, for he sees clearly that private property engenders class antagonism and disharmony. Therefore "men and women are to have a common way of life. . . —common education, common children; and they are to watch over the citizens in common."

Some researchers, such as Cordelia Fine, argue that available evidence does not support a biological basis for gender roles.

Evolutionary perspective

Based on the current theories and research on the sexual division of labor, four critical aspects of hunter‐gatherer socioecology led to the evolutionary origin of the SDL in humans: (1) long‐term dependency on high‐cost offspring, (2) optimal dietary mix of mutually exclusive foods, (3) efficient foraging based on specialized skill, and (4) sex‐differentiated comparative advantage in tasks. These combined conditions are rare in nonhuman vertebrates but common to currently-existing populations of human foragers, which, thus, gives rise to a potential factor for the evolutionary divergence of social behaviors in Homo.

Hunting hypothesis

From Wikipedia, the free encyclopedia

https://en.wikipedia.org/wiki/Hunting_hypothesis

In paleoanthropology, the hunting hypothesis is the hypothesis that human evolution was primarily influenced by the activity of hunting for relatively large and fast animals, and that the activity of hunting distinguished human ancestors from other hominins.

While it is undisputed that early humans were hunters, the importance of this fact for the final steps in the emergence of the genus Homo out of earlier australopithecines, with its bipedalism and production of stone tools (from about 2.5 million years ago), and eventually also control of fire (from about 1.5 million years ago), is emphasized in the "hunting hypothesis", and de-emphasized in scenarios that stress the omnivore status of humans as their recipe for success, and social interaction, including mating behaviour as essential in the emergence of language and culture.

Advocates of the hunting hypothesis tend to believe that tool use and toolmaking essential to effective hunting were an extremely important part of human evolution, and trace the origin of language and religion to a hunting context.

As societal evidence David Buss cites that modern tribal population deploy hunting as their primary way of acquiring food. The Aka pygmies in the Central African Republic spend 56% of their quest for nourishment hunting, 27% gathering, and 17% processing food. Additionally, the !Kung in Botswana retain 40% of their calories from hunting and this percentage varies from 20% to 90% depending on the season. For physical evidence Buss first looks to the guts of humans and apes. The human gut consists mainly of the small intestines, which are responsible for the rapid breakdown of proteins and absorption of nutrients. The ape's gut is primarily colon, which indicates a vegetarian diet. This structural difference supports the hunting hypothesis in being an evolutionary branching point between modern humans and modern primates. Buss also cites human teeth in that fossilized human teeth have a thin enamel coating with very little heavy wear and tear that would result from a plant diet. The absence of thick enamel also indicates that historically humans have maintained a meat-heavy diet. Buss notes that the bones of animals human ancestors killed found at Olduvai Gorge have cut marks at strategic points on the bones that indicate tool usage and provide evidence for ancestral butchers.

Applications

Sexual division of labor (evolutionary perspective)

According to the hunting hypothesis, women are preoccupied with pregnancy and dependent children and so do not hunt because it is dangerous and less profitable. Gijsbert Stoet highlights the fact that men are more competent in throwing skills, focused attention, and spatial abilities. (Experiments 1 and 2). Another possible explanation for women gathering is their inherent prioritization of rearing offspring, which is difficult to uphold if women were hunting.

Provisioning hypothesis

Parental investment

Buss purports that the hunting hypothesis explains the high level of human male parental investment in offspring as compared to primates. Meat is an economical and condensed food resource in that it can be brought home to feed the young, however it is not efficient to carry low-calorie food across great distances. Thus, the act of hunting and the required transportation of the kill in order to feed offspring is a reasonable explanation for human male provisioning.

Male coalitions

Buss suggests that the Hunting hypothesis also explains the advent of strong male coalitions. Although chimpanzees form male-male coalitions, they tend to be temporary and opportunistic. Contrastingly, large game hunters require consistent and coordinated cooperation to succeed in large game hunting. Thus male coalitions were the result of working together to succeed in providing meat for the hunters themselves and their families. Kristen Hawkes suggests further that obtaining resources intended for community consumption increases a male's fitness by appealing to the male's society and thus being in the good favor of both males and females. The male relationship would improve hunting success and create alliances for future conflict and the female relationship would improve direct reproductive success. Buss proposes alternate explanations of emergence of the strong male coalitions. He suggests that male coalitions may have been the result of group-on-group aggression, defense, and in-group political alliances. This explanation does not support the relationship between male coalitions and hunting.

Hawkes proposes that hunters pursue large game and divide the kill across the group. Hunters compete to divvy up the kill to signal courage, power, generosity, prosocial intent, and dedication. By engaging in these activities, hunters receive reproductive benefits and respect. These reproductive benefits lead to greater reproductive success in more skilled hunters. Evidence of these hunting goals that do not only benefit the families of the hunters are in the Ache and Hadza men. Hawkes notes that their hunting techniques are less efficient than alternative methods and are energetically costly, but the men place more importance on displaying their bravery, power, and prosocial intent than on hunting efficiency. This method is different as compared to other societies where hunters retain the control of their kills and signal their intent of sharing. This alternate method aligns with the coalition support hypothesis, in efforts to create and preserve political associations.

Reciprocal altruism

The meat from successful large game hunts are more than what a single hunter can consume. Further, hunting success varies by week. One week a hunter may succeed in hunting large game and the next may return with no meat. In this situation Buss suggests that there are low costs to giving away meat that cannot be eaten by the individual hunter on his own and large benefits from the expectation of the returned favor in a week where his hunting is not successful. Hawkes calls this sharing “tolerated theft” and purports that the benefits of reciprocal altruism stem from the result that families will experience “lower daily variation and higher daily average” in their resources.

Provisioning may actually be a form of sexual competition between males for females. Hawkes suggests that male provisioning is a particularly human behavior, which forges the nuclear family. The structure of familial provisioning determines a form of resource distribution. However, Hawkes does acknowledge inconsistencies across societies and contexts such as the fluctuating time courses dedicated to hunting and gathering, which are not directly correlated with return rates, the fact that nutrition value is often chosen over caloric count, and the fact that meat is a more widely spread resource than other resources.

The show-off hypothesis

The show-off hypothesis is the concept that more successful men have better mate options. The idea relates back to the fact that meat, the result of hunting expeditions, is a distinct resource in that it comes in large quantities that more often than not the hunter's own family is not able to consume in a timely manner so that the meat doesn't go sour. Also the success of hunting is unpredictable whereas berries and fruits, unless there is a drought or a bad bush, are fairly consistent in seasonality. Kristen Hawkes argues that women favor neighbors opting for men who provide the advantageous, yet infrequent meat feasts. These women may profit from alliance and the resulting feasts, especially in times of shortage. Hawkes suggests that it would be beneficial for women to reward men who employ the “show-off strategy” by supporting them in a dispute, caring for their offspring, or providing sexual favors. The benefits women may gain from their alignment lie in favored treatment of the offspring spawned by the show-off from neighbors. Buss echoes and cites Hawke's thoughts on the show-off's benefits in sexual access, increased likelihood of having children, and the favorable treatment his children would receive from the other members of the society. Hawkes also suggests that show-offs are more likely to live in large groups and thus be less susceptible to predators. Show-offs gain more benefits from just sharing with their family (classical fitness) in the potential favorable treatment from the community and reciprocal altruism from other members of the community.

Hawkes uses the Ache people of Paraguay as evidence for the Show-off hypothesis. Food acquired by men was more widely distributed across the community and inconsistent resources that came in large quantities when acquired were also more widely shared.

While this is represented in the Ache according to Hawkes, Buss notes that this trend is contradicted in the Hadza who evenly distribute the meat across all members of their population and whose hunters have very little control over the distribution. In the Hadza the show-off hypothesis does not have to do with the resources that result from hunting, but from the prestige and risk that is involved in big game hunting. There are possible circuitous benefits such as protection and defense.