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Abstract – In 1948, Angus J. Bateman reported a stronger relationship between mating and reproductive success in male fruit flies compared with females, and concluded that selection should universally favour ‘an undiscriminating eagerness in the males and a discriminating passivity in the females’ to obtain mates.

1. The conventional view of promiscuous, undiscriminating males and coy, choosy females has also been applied to our own species.
2. Here, we challenge the view that evolutionary theory prescribes stereotyped sex roles in human beings, firstly by reviewing Bateman’s principles and recent sexual selection theory and, secondly, by examining data on mating behaviour and reproductive success in current and historic human populations.

We argue that human mating strategies are unlikely to conform to a single universal pattern. In The Descent of Man, Charles Darwin noted that, throughout the animal kingdom, ‘the males of almost all animals have stronger passions than the females. Hence it is the males that fight together and sedulously display their charms before the female’ (Ref.

P.272). Darwin erroneously suggested that eagerness of males ultimately resulted from the lower costs of transporting small sperm compared to the costs of moving relatively larger eggs, The first compelling explanation of why competitiveness (see Glossary ) and choosiness might differ between the sexes was provided by Bateman in an experimental study of fruit flies ( Drosophila melanogaster ).

Bateman’s famous experiments showed that the number of offspring fathered by a male Drosophila increased with his number of mates, whereas a female fruit fly did not gain an increase in number of offspring from mating with several males. Bateman concluded that, because single ova are more costly to produce than are single sperm, the number of offspring produced by a female fruit fly was limited mainly by her ability to produce eggs, whereas the reproductive success of a male was limited by the number of females that he inseminated.

He also stated that, in our own species, the sex difference in gamete size would result in greater within-sex competition amongst males than females, The importance of Bateman’s idea to evolutionary theory was brought to prominence by Robert Trivers, who drew attention to postzygotic parental investment, such as feeding young and defence against predators.

Trivers predicted that the sex with the largest parental investment, usually female, would become a limiting resource for which members of the other sex compete. When females invest more than males, the ratio of reproductively available males to females (the operational sex ratio ) is assumed to be male-biased.

• In these situations, reproductive success would be expected to vary more amongst males than females, with females competing less intensely for mates and seeking out fewer partners than males,
• Apparently in support of this argument, greater variance in male than female reproductive success has been reported in some insects, frogs, lizards, birds and mammals,

Conversely, in sex-role-reversal species with high levels of paternal investment, females are predicted to compete more intensely than males for mates because males limit female reproductive success, The aim of this paper is to review data on variance in reproductive and mating success and on the shape of the relationship between these variables in current and historic human populations, and to consider the implications of variation between populations for our understanding of human sex roles.
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What is Bateman’s principle What implications does it have for sexual selection?

Description – Typically it is the females who have a relatively larger investment in producing each offspring. Bateman attributed the origin of the unequal investment to the differences in the production of gametes: sperm are cheaper than eggs. A single male can easily fertilize all of a female’s eggs; she will not produce more offspring by mating with more than one male.

1. A male is capable of fathering more offspring if he mates with several females.
2. By and large, a male’s potential reproductive success is limited by the number of females he mates with, whereas a female’s potential reproductive success is limited by how many eggs she can produce.
3. According to Bateman’s principle, this results in sexual selection, in which males compete with each other, and females become choosy in which males to mate with.

Thus, as a result of being anisogamous, males are fundamentally promiscuous, and females are fundamentally selective.
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What are the key concepts of sexual selection?

sexual selection, theory in postulating that the evolution of certain conspicuous physical traits—such as pronounced coloration, increased size, or striking adornments—in animals may grant the possessors of these traits greater success in obtaining mates.

From the perspective of natural selection, such increases in mating opportunities outweigh the risks associated with the animal’s increased visibility in its environment, This concept was initially put forth by English naturalist Charles Darwin in The Descent of Man (1871). Mutual attraction between the sexes is an important factor in reproduction,

The males and females of many animal species are similar in size and shape except for the sexual organs and secondary sexual characteristics such as the breasts of female mammals, There are, however, species in which the sexes exhibit striking dimorphism (or physical difference).

Particularly in birds and mammals, the males are often larger and stronger, more brightly coloured, or endowed with conspicuous ornamentation. These traits, however, make animals more visible to predators—the long plumage of male peacocks ( Pavo cristatus ) and birds of paradise ( Paradisaea ) and the enormous antlers of aged male deer ( Odocoileus ) are cumbersome loads in the best of cases.

Darwin knew that natural selection could not be expected to favour the evolution of disadvantageous traits, and he was able to offer a solution to this problem. He proposed that such traits arise by “sexual selection,” which “depends not on a struggle for existence in relation to other organic beings or to external conditions but on a struggle between the individuals of one sex, generally the males, for the possession of the other sex.” More From Britannica evolution: Sexual selection The concept of sexual selection as a special form of natural selection is easily explained. Other things being equal, organisms more proficient in securing mates have higher fitness. There are two general circumstances leading to sexual selection.

• One is the preference shown by one sex (often the females) for individuals of the other sex that exhibit certain traits.
• The other is increased strength (usually among the males) that yields greater success in securing mates.
• The presence of a particular trait among the members of one sex can make them somehow more attractive to the opposite sex.

This type of “sex appeal” has been experimentally demonstrated in all sorts of animals, from vinegar flies ( Drosophila ) to pigeons, mice, dogs ( Canis lupus familiaris ), and rhesus monkeys ( Macacca mulatta ). When, for example, Drosophila flies, some with yellow bodies as a result of spontaneous mutation and others with the normal yellowish gray pigmentation, are placed together, normal males are preferred over yellow males by females with either body colour,

Sexual selection can also come about because a trait—the antlers of a stag, for example—increases prowess in competition with members of the same sex. Stags, rams, and bulls use antlers or horns in contests of strength; a winning male usually secures more female mates. Therefore, sexual selection may lead to increased size and aggressiveness in males.

Male baboons ( Papio ) are more than twice as large as females, and the behaviour of the docile females contrasts with that of the aggressive males. A similar dimorphism occurs in the northern sea lion, Eumetopias jubata, where males weigh about 1,000 kg (2,200 pounds), about three times as much as females.

The males fight fiercely in their competition for females; large, battle-scarred males occupy their own rocky islets, each holding a harem of as many as 20 females. Among many mammals that live in packs, troops, or herds—such as wolves, horses, and buffaloes—there usually is a hierarchy of dominance based on age and strength, with males that rank high in the hierarchy doing most of the mating.

Francisco Jose Ayala
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What did Bateman’s influential study of Drosophila reproduction show?

Bateman said his results showed that male number of mates (NM) was more variable than female NM; male reproductive success (RS) was more variable than female RS; and RS in males, but not in females, was because of NM.
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What is the Bateman’s principle?

Abstract – Bateman’s principle, which states that male reproductive success should increase with multiple mating, whereas female reproductive success should not, has long been used to explain sex differences in behavior. The statistical relationship between mating success and reproductive success, or Bateman gradient, has been proposed as a way to quantify sex differences in sexual selection.

We used a long-term data set on the distribution of paternity in the socially monogamous dark-eyed junco to examine the effect of multiple mating on lifetime reproductive success and to determine the relative contributions of within-pair and extra-pair mating. Both sexes exhibited a strong positive Bateman gradient, even when the number of breeding years was accounted for.

Although theory suggests that this pattern indicates a strong potential for sexual selection in both sexes, we argue that the interpretation of strong Bateman gradients, particularly in females, has many potential complications. We discuss several alternative explanations for our results, none of which requires sexual selection acting on female traits, including targeting of inherently fecund females by males seeking extra-pair mates and increased power to detect extra-pair offspring as family size increases.
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What is the problem with Bateman’s principle?

What the Repetition Discovered – Our repetition appears to be unique in that we tried to replicate exactly Bateman’s methodology of parentage assignment as far as we could. We used the same mutant lines Bateman used. In our study, we cultured adult subjects as Bateman had done, so that each expressed a unique genetically-determined marker phenotype ( Fig.3A and B ).

Table S1 in our original report 30 illustrates that each adult subject was genetically and phenotypically distinct; that is, (regardless of their sex) in each of our replicated populations, each adult carried a single allele at its marker locus, while having only wild-type alleles at all other subjects’ marker loci.

We included the cultured adults in experimental populations in the same combinations of sexes, markers per sex, age of males and females and duration of the period during which mating could occur that Bateman reported (see Table S1 in ref.30 ). Figure 3. A stylized view of offspring genotypes ( A ) and observable offspring phenotypes ( B ) when each parent is a heterozygote dominant at a unique marker locus and wild type at the other parent’s marker locus. In both panels capital letters indicate dominant alleles and lower case indicates wild-type alleles for two parents each with a dominant marker allele each at a different locus.

The male’s maker locus is indicated by “B” and the female’s by “R.” Wild-type alleles at mother’s marker locus are indicated by lowercase, “r” and at father’s marker locus by lowercase “b.” In ( B ) the bolded letters indicate visible mutations. Following Bateman’s method closely, we counted the number of mates using only the offspring with a mutation from each parent, the double mutant offspring, M ♀ M ♂ s.

According to Bateman, M ♀ M ♂ s allowed an unbiased count of how many mates the subject adults had. Like Bateman we used the sum of the double mutant offspring plus the single mutant offspring (those with a marker mutation from one parent only) as an estimate of the number of offspring for each subject adult (see Fig.1 ).

• Like Bateman we did not watch the mating behavior of our subjects, so we had no better estimate of who mated with whom than Bateman did.
• Thus, the veracity of Bateman’s study and our replication turned on the “fairness” of the parental markers: Were they neutral with respect to Bateman’s goals of inferring number of mates and number of offspring for each subject? This question is one that modern forensic scientists and those studying genetic parentage also must do and do in fact address.

If markers fail to fit Mendel’s rules or Hardy-Weinberg expectations or are otherwise non-neutral, modern geneticists exclude particular loci from use in their studies of forensics, kinship, and genetic parentage.31, 32 Bateman-era geneticists would have used the simple expectations from a consideration of Mendelian principles to test the fairness of the markers ( Figs.2 and ​ 3 ): Bateman did test if half the offspring could be assigned to mothers and half to fathers, and concluded that there was no statistical difference in the representation among offspring of mothers’ vs.

• Fathers’ marker phenotypes.
• However, if he tested whether the frequency of double mutant offspring was unbiased, he did not report it.
• It appears he did not test his data against Mendel’s expected frequencies as his Table 4 ( Fig.1 ) data clearly significantly depart from Mendelian frequencies.
• Such a test of the frequency of adult markers in offspring is the decisive one required for demonstration that estimates of number of mates per individual and the V NM were unbiased, fairly representing who did and did not mate.

Assuming Mendelian inheritance of alleles when each parent is heterozygous dominant at unique loci ( Fig.1 ), there should be 25% of offspring with both parental mutations, 25% with the dominant allele at mother’s marker locus but a wild-type allele at father’s marker locus, 25% with the wild-type allele at mother’s marker locus and the dominant allele at father’s marker locus and 25% with the wild-type allele at each of their parents’ marker loci ( Figs.2 and ​ 3 ).

We generalize these types of offspring phenotypically as M ♀ M ♂, M ♀ w ♂, w ♀ M ♂ and w ♀ w ♂, respectively. The frequency of M ♀ M ♂ offspring was significantly lower than expected overall.30 The fatal flaw that our repetition revealed is that the method miscounts the number of mates for each sex—key variables in Bateman’s study—to an unknown degree, because in Bateman’s study the only information about who mated with whom was from the phenotypes of the M ♀ M ♂ offspring.

Using Bateman’s method we coded some subjects as having zero mates, when they in fact had one or more mates, which was clear when we observed “zero mated subjects” whose phenotypes appeared in their single mutant—M ♀ w ♂ and w ♀ M ♂ —offspring ( Fig.4 ). Figure 4. Subjects seemingly without mates had offspring, which is highly unlikely in a sexually reproducing diploid species. Reproductive success counted as the sum of M ♀ M ♂ plus M ♀ w ♂ for female subjects ( A ) and as M ♀ M ♂ plus w ♀ M ♂ for male subjects ( B ) against the number of mates counted from M ♀ M ♂ offspring for females ( A ) and for males ( B ) exposes a biological impossibility.

• Bateman’s method overestimates the number of individuals with zero mates (21 subjects among females and 43 among males), thereby underestimating the number with one or more mates.
• The magnitude of error among male subjects (43 males out of a total N of 166 males) was greater than among female subjects (21 females out of a total N of 166 females), which would have falsely increased the V NM estimates of males relative to females.

We use these plots to illustrate one of the most egregious errors in Bateman’s method: subjects who seemed to have no mates had offspring. The second flaw arose because significantly more single mutant offspring survived when they had their mother’s wild-type allele and their father’s mutant allele (that is, the w ♀ M ♂ s) than offspring with their mother’s marker allele and their father’s wild-type allele (the M ♀ w ♂ s), the sex differences in reproductive success were also biased, showing higher RS for fathers than for mothers.

• Although Bateman did report that the numbers of offspring from M ♀ w ♂ and w ♀ M ♂ were about equal and his Table 4 ( Fig.1 ) suggested statistical equality in RS for assigned parents, he did not report the frequency of M ♀ M ♂ s or the test for parental equality of RS in his entire experiment.
• Had he reported a test of observed frequencies of M ♀ M ♂, M ♀ w ♂, w ♀ M ♂ and w ♀ w ♂ against Mendel’s expectations of M ♀ M ♂, M ♀ w ♂, w ♀ M ♂ and w ♀ w ♂, he would have provided the information that his contemporaries and modern readers needed to evaluate the reliability of his markers given his questions.

Although it appeared to be “cutting edge” in its day, the methodology of Bateman’s study appears to have been fatally flawed. Our replication showed that using Bateman’s method produced two observations that are biologically impossible or at least extremely unlikely.

Figure 4 shows the first by examining inferences about NM and RS for the 166 female subjects (A) and 166 male subjects (B) in the replication. The x-axis is the number of mates for subjects counted from M ♀ M ♂ offspring, the only offspring providing information about who mated with whom. The y-axis is reproductive success counted as the ∑ = M ♀ M ♂ + M ♀ w ♂ (for female subjects, the mothers) or ∑ = M ♀ M ♂ + w ♀ M ♂ (for male subjects, the fathers).

A single fact exposes the bias in Bateman’s method: Some individuals that we counted using Bateman’s method as having zero mates nevertheless, using Bateman’s method, had offspring ( Fig.4 ). The mismatch between information in double mutant and single mutant offspring was due in our experiment to significantly lower viability of M ♀ M ♂ offspring.

• Remember that single mutant offspring inform questions about how many offspring each subject had, but they are silent about who mated with whom.
• Because of the inviability of double mutant offspring, some adults were scored as having zero mates, when in fact that had some unknown number of mates.
• The resultant miscount incorrectly increased the number of males in the class having zero mates, and the number with ≥ 1 was consequently underestimated.

Using the method Bateman used, Figure 4 shows that Bateman would have incorrectly assigned many more males than females to the zero class of number of mates, so that the effect would be to increase the male V NM relative to the effect on female V NM,

There is no way to know what effect the incorrect assignment of subjects to the zero mating class has on the under-estimation of the subjects in the classes with ≥ 1 mate ( Fig.4 ). The second biological impossibility that our replication revealed was that there was a systematic bias in counts of offspring with fathers vs.

mothers. That is, using Bateman’s method we were able to assign genetic paternity significantly more often than genetic maternity, making it seem as though more offspring had fathers than mothers, verifying that there was something wrong with the methodology, just as we 12 had earlier suspected.

• More paternal assignments occurred because the number of w ♀ M ♂ offspring was greater than the number of M ♀ w ♂ offspring.
• We tested for significance differences with a plot of the difference scores in the apparent number of offspring with fathers minus the apparent number with mothers (see Fig.1 in ref.30 ).

Because the bias resulted in assigning more fathers than mothers as parents, the estimate of RS was greater for fathers than mothers, demonstrably because of mismeasurements derived from Bateman’s method: single mutant offspring who inherited the dominant allele from their mother’s marker locus plus a wild-type allele at their fathers had lower viability than offspring who inherited a dominant allele from their father’s marker locus but a wild-type from their mother’s marker locus.

• Systematic, methodological mismeasurement of number of mates and number of offspring leaves open to question Bateman’s conclusion that there is an enhanced effect of RS as a function of NM for males, but not females.
• Because of the bias in the methodology, our repetition could not address the main questions that Bateman set out to answer.

If his overall data, not just the data in his Table 4 ( Fig.1 ), were inadequate to his questions as our repetition suggests, his answers to his questions would be unreliable as well.
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What is sexual selection a key concept of the evolutionary psychology approach?

From an ultimate, evolutionary perspective, sexual selection selects for behaviors that will increase the likelihood of finding a mate and producing offspring, resulting in the flow of genetic material through the generations. Sexual selection has encouraged costly signaling.
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What is the principle underlying sexual selection and sexual conflict?

Notes –

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What is the Bateman’s gradient?

Discussion – We have seen that completely symmetrical models of fertilisation and multiple mating can reproduce the salient features of Bateman gradients without invoking any sex-specific assumptions aside from the definitional gametic imbalance. The only sex-specific property included in Models 1 and 2 is a difference in gamete number, a fundamental property of the two sexes.

Although the biological definition of the two sexes is commonly stated in terms of gamete size, a difference in gamete size translates to a difference in gamete number where the latter is often modelled as an inverse of gamete size, particularly in models of the ancestral origin of the two sexes 8 (it should be noted that in many contemporary organisms subsequent selection has led to a situation where total gamete volume is higher in females than in males 28, 29, but gamete number is nevertheless higher in males).

Here the central aim has been to analyse the effect of a difference in gamete number while excluding all other sex differences and complications which are not directly relevant to the question. By excluding all other possible causes, I have validated Bateman’s 1 assertion that a difference in gamete numbers between the sexes alone causes a difference in Bateman gradients between the sexes.

In Model 3 I have included one sex-specific assumption beyond gamete number: internal fertilisation, such that females are gamete recipients and males are gamete donors, and the model shows that when fertilisation is efficient, conclusions drawn from the symmetrical models remain valid despite the introduction of this additional asymmetry.

Inefficient fertilisation (small parameter a in the models) and consequently strong gamete limitation can alter the results under both external and internal fertilisation but in different ways. Gamete limitation can bring Bateman gradients back towards equality in external fertilisers even when gamete numbers are asymmetrical, but not reverse them (Figs.1 and 2 ).

A similar effect of diminishing the sex difference in Bateman gradients arises when the number of matings and polygamy increases at the population level (Fig.4 ), in line with earlier theoretical results 2, However, a combination of inefficient fertilisation and relatively small differences in gamete numbers between the sexes can theoretically reverse Bateman gradients under internal fertilisation (Fig.3 ).

Gamete limitation is not uncommon in external fertilisers in nature 30, 31, and the equalising effect seen in Figs.1 and 2 may be significant for some external fertilisers. Similarly, the equalising effect seen in Fig.4 seems plausible in polyandrous internally fertilising species.

The reversal of Bateman gradients seen in Fig.3 is more subtle. Sperm limitation is known to occur in internal fertilisers, but this is typically a consequence of male multiple mating 32, The converse, where the evolution of multiple mating would be driven by sperm limitation in sperm recipients from a hypothetical ancestral state of monogamy then seems less likely and calls for further theoretical investigation.

The novel observation that gamete limitation can in theory reverse Bateman gradients under internal fertilisation is therefore a very interesting one and shows that Bateman’s seemingly simple assertion is far from trivial or obvious, even if broadly correct in its logic.

Empirically, it has nevertheless been shown that Bateman gradients are steeper in males than in females in most animal species 27, although exceptions are not as uncommon as Bateman’s writing might suggest 3, 27 (in fairness, Bateman did claim the difference in Bateman gradients to be “almost universal” 1 ).

Fig.4: The Bateman functions of Eqs. ( 2 )–( 4 ) when the resident number of matings varies. The gametic system is anisogamy with n x  = 100 (female, indicated by blue crosses and connecting lines), n y  = 100,000,000 (male, indicated by black dots and connecting lines). The number of resident matings m varies between a – d as indicated above the panels.

• Results are visually indistinguishable for Models 2-3 and with fertilisation efficiency parameters a  = 0.001/ a  = 1.
• Increased number of resident matings (i.e., increased gamete competition) decreases the steepness of the male Bateman gradient but does not eliminate the asymmetry between female and male gradients, in line with earlier theoretical results by Parker and Birkhead 2,

A more abstract view of the models provides further insight into the source of the asymmetry in selection. First, note that all three models contain a fertilisation function f and that typically a fertilisation function can be written using an alternative probabilistic notation: f(N x, N y )  =  N x   p x (N x, N y ) =  N y   p y (N x, N y ) 19, or written more concisely, f  =  N x   p x  =  N y   p y where p x and p y indicate the per-gamete fertilisation probabilities of gametes of the two types.

These equations imply that in any given fertilisation event the probability must be smaller for the more numerous gamete type and can indeed approach the maximum value of 1 for the less numerous gamete type 12, It therefore seems intuitively plausible that in a situation that is otherwise symmetrical for the two sexes, the producer of the less numerous gametes (female) has less scope to increase this probability which explains the asymmetry in Figs.1 and 2,

In the present models, there are two ways in which individuals can potentially increase p x or p y and thus their number of fertilised gametes. The focal individual can monopolise gametes from a larger number of opposite type individuals (Model 1 and the gamete recipient side of Model 3).

1. Alternatively, the focal individual can spread its own gametes over a larger number of fertilisation events (Model 2 and the gamete donor side of Model 3).
2. In both cases the absolute number of accessible gametes of the opposite type increases, and when fertilisation is efficient, the sex producing the larger number of gametes (males) has more to gain from this increase.

However, when fertilisation is inefficient, it is not just the absolute number of gametes that matters, but also their concentration or density. In Model 3, only females can increase the concentration of male gametes around their own gametes: when a female mates multiply in this model, the concentration of sperm around her eggs increases proportionally to the number of mates.

1. When a male mates multiply in the same model, there is no such concentration effect, and instead, he dilutes his own gametes across a larger number of females whose egg concentration remains unchanged.
2. This difference explains the reversal of Bateman gradients in Model 3 when fertilisation is inefficient: only females can improve fertilisation efficiency by mating multiply.

A somewhat ambiguous aspect of Bateman’s 1 writing is the claim that the asymmetry arises from competition between male gametes for the fertilisation of the female gametes: “The primary cause of intra-masculine selection would thus seem to be that females produce much fewer gametes than males.

Consequently, there is competition between male gametes for the fertilisation of the female gametes. And this competition is vastly more intense than that hitherto considered between zygotes”. Bateman does not specify whether this means direct gamete competition or indirect competition for fertilisations.

For example, Model 2 includes direct gamete competition among individuals of both types, whereas in Model 1 a mutant monopolising gamete of the opposite type faces no direct gamete competition, nor does a gamete recipient in Model 3. Selection, in general, requires competition in the sense of within-population variation in reproductive success, but from a logical perspective, the asymmetry in Bateman gradients does not necessitate direct competition between gametes of different individuals.

1. In fact, polygamy and the resulting gamete competition tend to reduce (although not reverse) the difference between the male and female Bateman gradients (Fig.4 ), in line with previous theoretical work 2,
2. A more general explanation for the difference in Bateman gradients is simply that the producer of the more numerous gametes has more to gain by increased access to opposite type gametes, irrespective of the presence of competing gametes from other individuals (but see above for exceptions when internal fertilisation, inefficient fertilisation, and relatively low ratios of gamete numbers are combined).

Bateman’s work has been widely criticised in recent years 10, 33, 34, 35, Experimental methods have inevitably moved on over seven decades, making Bateman’s approach outdated. Yet, as has been noted by others, Bateman’s general conclusions are not necessarily negated by scrutiny of empirical methods, just as Mendel’s experiments are not worthless despite their problems 2,

What is even more clear is that the conceptual framework initiated by Bateman’s work retains value despite disagreements regarding experiments and their interpretation. This article has revisited one aspect of this conceptual framework, and one that Bateman based purely on verbal argument 1 : I have shown that Bateman’s assertion relating gamete number to the Bateman gradient and to sexual selection is correct under fairly general conditions, but not inevitable.

Given that Bateman’s assertion explicitly relates gamete numbers to reproductive success with no mathematical justification, a natural step forward is to use the mathematical machinery that has been developed for relating gamete numbers to fertilisation success since Bateman published his work—namely, fertilisation functions 19,

At the most general level, fertilisation functions can be derived from biophysical principles in a manner that is completely agnostic regarding sexes 19, 24, 36, allowing model construction that makes no sex-specific assumptions and thus avoids concerns relating to such assumptions and possible associated biases 9,

Any difference between the sexes arising in such a model must ultimately trace back to the gametic level. An additional purpose served by fertilisation functions here is that they permit modelling variation in fertilisation efficiency while maintaining consistency in the models (Figs.1 – 3 ; note also that fertilisation efficiency could itself be causally linked to other factors, such as gamete size or motility 37, and the structure of the present models makes such potential future modifications straightforward).

Analysing the logical validity of Bateman’s assertion is important for at least three reasons. Firstly, it shows that Bateman’s assertion is far from obvious or trivial and that the argument is subtle, particularly under internal fertilisation. Second, it strengthens the mathematical foundations of Batemans’s contested work, showing that despite exceptions, under fairly general conditions Bateman’s assertion was correct.

Third, it adds to our understanding of the ‘sexual cascade’ and the mainstream direction of selection in the evolutionary history of sexual reproduction 38, by showing why Bateman gradients are typically expected to diverge as a consequence of the evolution of anisogamy (which likely evolved under external fertilisation), thus linking Bateman gradients to the most fundamental biological definition of the two sexes 8,
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What are the 4 reasons why Drosophila was chosen?

The four reasons for which Morgan has chosen Drosophila for his experiments in genetics are as follows: (i) Drosophila has a very short life cycle i.e. of 2-weeks. (ii) It can be grown easily in the laboratory. (iii) In single mating it produces a large number of flies.
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What were the results of the Drosophila experiment?

Chromosomal theory of inheritance – After a frustrating and fruitless two-year search for Drosophila with different characteristics, white-eyed flies suddenly appeared among Thomas Morgan’s normal, red-eyed flies. To find out more about these white-eyed flies, Thomas carried out crosses between them and the red-eyed flies.

• Through these early experiments he found that all of the white-eyed flies being produced were males, there were no white-eyed females at all.
• Inheritance of the white-eye trait might have a basis in the chromosomes, more specifically, the sex chromosomes.
• After further crosses Thomas observed that the female flies only showed the white-eyed trait if they inherited two copies of the mutant genes, but males only needed one copy of the mutant gene to have white eyes.

This suggested to him that inheritance of the white-eye trait might have a basis in the chromosomes, more specifically the sex chromosomes, At that time, little was known about the sex chromosomes, although it was thought that one of the Drosophila’s four chromosome pairs was likely to be involved in sex determination.

Thomas continued his work looking at a number of different traits in the Drosophila and in 1915 he published his theory Mechanism of Mendelian Heredity, acknowledging that he agreed with Mendel’s concept of dominant and recessive traits. In his work he introduced the concept of genes carrying hereditary information and explained the discovery that certain characteristics were linked to sex.

He also revealed that different combinations of traits arise from changes occurring in the chromosomes during reproduction. Thomas Morgan received the Nobel Prize for Medicine in 1933. In 1933 Thomas Morgan received the Nobel Prize for Medicine for his work in establishing the chromosomal theory of inheritance.
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What is the Bateman’s principle of polyandry?

Abstract – Bateman’s principle has been widely interpreted to imply that females gain no fitness benefits from polyandry (Bateman, 1948) and, therefore, should not be expected to mate multiply (here defined as mating with more than one male). Nevertheless, it is increasingly clear that females of many, if not most, taxa do copulate with multiple males (e.g.

Birkhead and Wier, 1998). Moreover, polyandry is widespread despite considerable costs, including wasted time and energy, increased risk of predation and disease, potential damage caused by male seminal fluids and copulatory organs, and even death (Keller and Reeve, 1995; Eberhard, 1996). Despite these associated costs, females of diverse taxa not only accept several mates but also actively solicit multiple copulations in many instances (Birkhead and Moller, 1998).

As evidence of diverse potential benefits associated with polyandry now accumulates, the assumption that females should not mate multiply because they cannot increase offspring numbers by doing so appears questionable. Importantly, since females have greater potential than males to influence the quality of their offspring, and investment in current reproduction has consequences for future reproductive attempts, they should be expected to optimise offspring numbers rather than maximise numbers produced in any given reproductive attempt (Roff, 1992; Stearns, 1992).
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What is Bateman’s principle quizlet?

Bateman’s principle. – variability in reproductive success is greater in males than in females.
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What is the purpose of sexual selection in evolution?

Discussion – Sexual selection is a much more powerful evolutionary force than natural selection because variation in mating success can magnify selection and simultaneously promote and maintain novel genetic variation among individuals, which ultimately fuels rapid evolutionary change.

• Interestingly, if an unsuccessful male on a peacock lek with lower-than-average fitness (as a result of deleterious mutations) gains no mates at all (normally the majority of males on a lek), then the net rate of evolutionary change on a phenotypic character is zero.
• Only when the relative fitness of a male is greater-than-average (as a result of a beneficial mutation) will selection result in rapid adaptive change since only these males will gain mates.

An increase in the rate of mutation via a mutator gene will therefore also only occur if the mutator gene is linked to a beneficial mutation which can hitch-hike into the population. The self-sustaining positive-feedback loop in the level of additive genetic variance that results from this process maintains the female preference for males that do nothing but show-off their good genes.

1. I don’t think that the precise form of the mate preference function used in the model is important.
2. Females do need to choose males and unless there are genetic differences between males there is no basis for female choice.
3. A non-linear preference function as well as a linear preference function in relation to male quality would in my opinion produce the same qualitative result.

The number of mates obtained by any one male, however, will quantitatively affect the strength of selection for the genetic characteristics of that male. Although the natural history underlying the model is based on inter-sexual selection or mate choice for males (epitomised by the lek mating system of peafowl) with a character that reveals their underlying genetic quality, there is no reason to believe that the fundamentals of this process cannot also be applied to intra-sexual selection, where the outcome of contests between individuals of the same sex determines mating success.

Wherever there is variance in mating success which is ultimately determined by variation in genetic quality then there is the opportunity for very rapid evolutionary change. Sexual selection when viewed in this way has the potential to explain other evolutionary problems ( Sheratt and Wilkinson, 2009 ) that are characterised by having impossibly large costs and no obvious immediate benefits and that have baffled evolutionary biologists for a long time, such as the evolution of sexual reproduction and the existence of males ( Smith, 1986 ; Agrawal, 2001 ; Siller, 2001 ; Whitlock and Agrawal, 2009 ; Roberts and Petrie, 2021 ).

The problem with the evolution of sexual reproduction can be briefly summed up as the cost of producing males. The number of offspring produced by an asexual female is twice that produced by a sexual female (producing equal numbers of male and female offspring) since males cannot produce offspring by themselves.

• In order to overcome this large numerical cost a sexually produced offspring must be twice as fit as an asexually produced offspring.
• Only if there are genetic differences between males in a population will it pay females to outbreed in order to exchange their male genes to increase the genetic quality of their offspring.

Both Agrawal (2001) and Siller (2001), modelled the effect of sexual selection on the production of males and, concluded that the function of males in a sexually reproducing population was to remove bad genes or reduce the genetic load of a population ( Whitlock and Agrawal, 2009 ).

If sexual selection functions in the way I have described above, then sexual selection for good genes will provide a short-term advantage to produce males and rapidly facilitate the evolution of sexual reproduction ( Roberts and Petrie, 2021 ). If sexual selection does facilitate rapid adaptation to a changing environment then it is very important that we understand the fundamentals of adaptive mate choice and guard against any disruption to this process.

This is especially true when thinking about the conservation of species facing rapid climate change ( Gosling and Sutherland, 2000 ) or adaptation to the emergence of new zoonotic diseases ( Zuk, 2002 ) such as Covid-19. Any process that interferes with a female’s ability to discriminate between potential mates is a threat to the fitness of a population.

• The prevention of adaptive female choice in humans can be imposed politically or by religious doctrine and this can and does occur in human populations.
• Arranged marriages, forced matings and excessive control of female behaviour in societies can result in sub-optimal, maladaptive matings which in turn can adversely influence offspring health.

The concomitant effect of these practices or of any environmental pollutants such as artificial chemicals and drugs on adaptive mate choice behaviour, is not routinely considered and, given the importance of gaining good genes for offspring survival to reproduction in all species, it strikes me that this is a major oversight.
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What is the main point of evolutionary psychology?

Key Takeaways: Evolutionary Psychology –

• The field of evolutionary psychology is based on the idea that human emotions and behaviors have been shaped by natural selection.
• According to evolutionary psychologists, the human brain evolved in response to specific problems that early humans faced.
• A core idea of evolutionary psychology is that the behavior of humans today can be better understood by thinking about the context in which early humans evolved.

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What is sexual selection selection?

Table 2 – Examples of Definitions of Sexual Selection from Darwin Onwards

Darwin 1859, p.88: “Sexual selection depends, not on a struggle for existence, but on a struggle between the males for possession of the females; the result is not death to the unsuccessful competitor, but few or no offspring.”

Darwin 1871, p.256: “We are, however, here concerned only with that kind of selection, which I have called 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.”

Huxley 1938, p.416: “Darwin’s theory of sexual selection was of the compound deductive-inductive type. Deductively he postulated: (1) that under certain circumstances there would occur a struggle between males for mates, and that the characters giving success in such a struggle would have sexually-selective value and would be perpetuated irrespective of their natural-selective value in the general struggle for existence; (2) that these characters would be of two main types, (a) those subserving male display, (b) those subserving combat between rival males, and that such characters could not be evolved except under the operation of sexual selection as defined by him. With regard to display characters, he further deduced a rudimentary esthetic sense in females, and also a process of female choice as between rival males.”

Ehrman 1972 (Chapter 6 in Campbell), p.106: “At present it seems best to simply define sexual selection as all mechanisms which cause deviations from panmixia,”

Crook 1972 (Chapter 9 in Campbell), p.264: Social selection “is primarily in relation to direct competition.” “Social selection results from ( a ) effects of competition between the subject and others of either sex with respect of commodities essential to survival in a situation that will allow an attempt at reproduction, ( b ) competition for access to preferred members of the opposite sex for mating and ( c ) effects of competition between subjects for access to commodities in the environment essential for the rearing of their young to reproductive age. Of these b is the process most commonly referred to as sexual selection.”,

Maynard Smith 1978 (Chapter 10 Sexual selection, in The Evolution of Sex), p.168: “As soon as aniosogamy has evolved, different selective forces may act on males and females; it is these differential forces with which I am concerned in this chapter.”,

West-Eberhard 1979, p222 and subsequently: West-Eberhard follows Darwin in viewing sexual selection as competition for mates, but also considers sexual selection a subset of social selection, with the latter characterized by competition within a social group for one or more resources (which might include mates). For example: “I agree with Mayr (1972, p.88) that “something rather important was lost” in the process of redefining fitness and erasing Darwin’s distinction between these two kinds of selection — just as something is lost by stretching the concept of sexual selection to make it suit new purposes which, however interesting in their own right, tend to obscure what Darwin was trying to say (for example, Ehrman’s1972, p.106, redefinition of sexual selection as “all mechanisms which cause deviations from panmixia,” or Maynard Smith’s, 1978, inclusion of all selection acting differently on the two sexes). When Darwin wrote about sexual selection he focused primarily on social competition for mates.”

Partridge and Halliday 1984 (Chapter 9 in Krebs & Davies, 2 nd edition), p.222: “It has long been obvious that the gametes produced in natural populations do not pair up at random. Leaving aside the obvious restrictions imposed by species and gender, some individuals may obtain more fertilizations than others, and particular types of parings may be more common than others. Such nonrandom mating is of fundamental evolutionary importance because different matings may have different fitness consequences.” Continued on p.225: “As Darwin was first to recognize, variance in the number of successful matings is the raw material for sexual selection, defined as selection on characters giving certain individuals an advantage over others of the same sex in obtaining successful matings.”

Andersson 1994, p.3: “According to Darwin (1871), sexual selection arises from differences in reproductive success caused by competition over mates.” Continued on p.8: “Sexual selection of a trait can therefore be viewed as a shorthand phrase for differences in reproductive success, caused by competition over mates, and related to the expression of the traits”; and p.9: “In spite of many suggestions to the contrary by leading biologists the term sexual selection in here restricted to competition over mates.”

Roughgarden et al.2006, p.965: “Since 1871, sexual selection theory has often been restated (4), yet contemporary definitions share Darwin’s central narrative: “We now understand Males, who can produce many offspring with only minimal investment, spread their genes most effectively by mating promiscuously. Female reproductive output is far more constrained by the metabolic costs of producing eggs or offspring, and thus a female’s interests are served more by mate quality than by mate quantity” (5). The reproductive social behavior of most species has not been studied, but a great many of those that have been do not conform to Darwinian sexual-selection templates. We suggest that sexual selection is always mistaken, even where gender roles superficially match the Darwinian templates.”

Kokko et al.2006, p.44: “Sexual selection: selection generated by differential access to opposite-sex gametes (or mates).”,

Ritchie 2007, p.80: “Sexual selection: the component of natural selection arising owing to variation in mating or fertilization success”

Carranza 2009, p.750: “In 1994, I proposed a definition for sexual selection as (page 380; translated from Spanish): ‘those natural selection forces that operate differently in males and females because of the strategies of the sexes’. This is simply to adopt the concept of sex-dependent selection as a modern use of the term sexual selection to investigate the evolution of differences between the sexes.”

Clutton-Brock 2009, p.8: Contrasts in the operation of sexual selection in the two sexes raise the question of whether adaptations to intrasexual competition in females should be regarded as products of sexual selection or natural selection. In The Descent of Man Darwin sometimes described ‘sexual’ selection as selection operating through intrasexual competition to reproduce and sometimes as selection operating through competition for mates, although the term is now most commonly restricted to selection operating through intrasexual competition for mating opportunities ( Andersson 1994 ). Because females more commonly need to compete for breeding opportunities than mating opportunities, defining sexual selection in terms of competition for mates has the effect of restricting its operation to males, creating unfortunate dichotomies where functionally similar traits are attributed to sexual selection if they occur in males but to natural selection if they occur in females. The most satisfactory solution might be to abandon the distinction between sexual and natural selection altogether and emphasize, instead, the contrasting ways in which selection operates in males and females ( Clutton-Brock 2007 ). However, the distinction between sexual and natural selection is so heavily entrenched that this is unlikely to occur and the most feasible alternative is probably to broaden the concept of sexual selection to include all selection processes operating through intrasexual competition for breeding opportunities in either sex ( Clutton-Brock 2007 ).”

Jones and Ratterman 2009 : “Darwin makes it clear that not all selection related to reproduction constitutes sexual selection, as primary sexual traits—like ovaries and testes—can evolve as a consequence of natural selection. Even though he never spells it out in so many words, Darwin’s working definition of sexual selection is essentially identical to the one used by Andersson and most other scientists studying sexual selection. In particular, ‘‘sexual selection arises from differences in reproductive success caused by competition for access to mates”, This definition admittedly focuses primarily on precopulatory sexual selection, so a more complete definition should also include postcopulatory processes, which can be accomplished by tagging the phrase ‘‘or fertilization opportunities” onto the end of Andersson’s definition.”

Kuijper et al.2012 : “Sexual selection is the process by which individuals compete for access to mates and fertilization opportunities.”

Safran et al.2013, p.644: “we define sexual selection as the result of the differential reproductive success that arises from competition for mates and access to fertilizations.”

Rosenthal 2017, p.503: “Sexual selection. A special case of natural selection: differential reproductive success due to the ability to secure matings and/or fertilization.”

Alonzo and Servedio 2019, Table 1 : Their table offers a similar sample of definitions of sexual selection, which (together with our examples above) highlights the challenge for the field of sexual selection.

First, a definition of sexual selection has been proposed that limits itself to mate choice by females or otherwise ( Roughgarden et al.2006 ). However, as pointed out above, such a definition of sexual selection is far too narrow, as it excludes intrasexual selection via both mating and sperm and egg competition.

• In particular, it neglects a very substantial body of work that has traditionally sat within the compass of sexual selection: that is intrasexual (such as male–male) contest competition for access to gametes ( Andersson 1994 ; Hardy and Briffa 2013 ).
• This component of sexual selection influences traits that are unlikely to have been favored by narrow-sense natural selection, such as horns and antlers ( Andersson 1994 ; Emlen 2008, 2014 ; see in particular the discussion in McCullough et al.2016 ).

Focusing on mate choice, although ignoring the intrasexual competition, also lacks conceptual coherence, as it focuses on one group of mechanisms that might influence or mediate within-sex mating competition, whilst not including others (a point made, albeit rather cryptically, by Fisher 1930, p.131–132).

1. Second, sexual selection is sometimes defined in terms of variation in reproductive success (for example in textbooks such as Avassar et al.2013 ; Clark et al.2018 ).
2. Whilst this is understandable in some ways, because mating and reproduction seem to go hand in hand, reproductive success is actually a much broader concept, representing an organism’s direct fitness (in an inclusive fitness framework) through all direct fitness components, including those related to longevity, fecundity, and parental care.

Informally, one has to survive to reproduce, as well as find mates, so reproductive success per se is too broad a concept to separate out sexual selection from other aspects of narrow-sense natural selection; all direct fitness collapses into reproductive success.

Unfortunately, perhaps the most-repeated of Darwin’s definitions of sexual selection carries with it the sense of “reproductive success,” stating as it does that sexual selection “depends on the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction” ( Darwin 1871, p.256; Table 2 ).

Taken at face value, this definition seems to focus on reproduction, rather than competition for mates (and then gametes). However, Darwin, in the preceding pages, discussed the difference between primary and secondary characters, noting that primary characters – which are needed to reproduce at all – are not the target of sexual selection, but secondary sexual characters are.

Darwin also noted that it is ” scarcely possible to decide ” how to identify primary versus secondary sexual characters or separate out the effects of natural or sexual selection. So, the difficulties in ascribing forms of selection to traits were appreciated from the very outset of the intellectual history of sexual selection ( Darwin 1871, p.254; see also Fisher 1930, p.132).

The relationship between reproductive success and sexual selection has been brought into renewed focus in recent years through a number of papers that have sought to redraw, or at least reexamine, ways in which sexual selection may influence females ( Clutton-Brock 2007, 2009, 2010, 2017 ; Rosvall 2011 ; Stockley and Bro-Jørgensen 2011 ; Tobias et al.2012 ).

From a series of observations of – mostly – vertebrates, the idea that individuals of a given sex compete between themselves for resources, or social status, crucial for reproduction has been suggested to be a form of sexual selection, with the idea that “reproductive competition” comes to replace or broaden the notion of “competition for mates.” The problem with bringing female-female competition for reproductive resources, or indeed male–male competition for such resources, into sexual selection is that much of what all organisms do – male or female – is to compete for resources that sooner or later contribute to variation in reproductive success.

In the broadest terms, this means that natural and sexual selection perfectly coincide, and the latter term becomes meaningless ( Clutton-Brock 2007, 2009 ; Shuker 2010 ). If we wished to be less broad, then we would have to decide, a priori, how “close” to reproduction the resource was, or the competition for it was, when saying whether or not that competition engenders natural or sexual selection.

Given that resource acquisition, and the life-history decisions that underlie how resources are allocated and competed for, may play out over the long-term (for example early-life effects: Lindström 1999 ; Jonsson and Jonsson 2011 ), teasing resource competition apart to assign to sexual or natural selection would be challenging.

Instead, we suggest that components of “natural selection” are about being able to enter and remain in the fertilization game, where competition for access to mates and their gametes occurs, and that “sexual selection” is about how well you succeed in that game when compared with other same-sex contestants.

Whilst fully recognizing the impact sexual selection has on the fitness of both sexes, we consider that competition for access to gametes is the focus of sexual selection, and that competition for resources – whether directly required for reproduction or not – is the focus of other components of fitness, unless the resource itself influences access to gametes.

We will return to this topic below. Another definition of sexual selection is again drawn from a particular reading of Darwin. Authors such as Padian and Horner have argued that sexual selection is characterized by sexual dimorphism of secondary sexual traits ( Padian and Horner 2011a, 2011b, 2014a, 2014b ; but see Knell et al.2013 ; Borkovic and Russell 2014 ; Clutton-Brock 2017 also discusses the links between sexual dimorphism and sexual selection).

Basing this idea on the detailed discussions of dimorphism given by Darwin, sexual selection is then defined either as the driver of sexual dimorphism, or only as occurring when there is sexual dimorphism (for example Padian and Horner 2014b ). Put another way, without sexual dimorphism, sexual selection cannot act (or be said to have acted).

This view of sexual selection, which we reject, has been discussed in particular in the paleontological literature, where evidence for sexual selection is notoriously difficult to find (for example Knell et al.2013 ; Mallon 2017 ; Hone and Mallon 2017 ; O’Brien et al.2018 ).

• However, that search is made harder still by stipulating a priori that fossils need to exhibit sexual dimorphism before sexual selection as a mechanism can come into play.
• Whilst there is much that could be discussed here, we will simply make the following points.
• First, there is clear evidence that sexual dimorphism can arise through narrow-sense natural selection on the sexes favoring ecological displacement ( Shine 1989 ; Fairbairn et al.2007 ).

Second, the requirement for sexual dimorphism would mean that sexual selection cannot occur in isogamous species with separate mating types, or indeed in simultaneous hermaphrodites. Third, there is clear evidence of sexual selection in species that are sexually monomorphic, such as mutual mate choice for head ornaments in crested auklets ( Jones and Hunter 1993 ).

• All in all, the requirement for sexual dimorphism for sexual selection to be said to be occurring is overly restrictive and lacks logical coherence when considering the competition for gametes in monomorphic species.
• Along similar lines, but not so closely tied to sexual dimorphism per se, another alternative definition focuses on the different patterns of selection that arise on the two sexes ( Carranza 2009 ), taking its cue from the title of Darwin’s book (1871: ” selection in relation to sex” ).

As noted above, we should be careful in reading too much into the title of that book, and indeed the phraseology Darwin used at times, given the social circumstances under which he was writing, and the pressures applied by his publisher ( Dawson 2007 ).

1. Nonetheless, it is still not clear that viewing sexual selection in terms of differential patterns of selection on males and females is useful.
2. Carranza (2009) argued for a definition of sexual selection based on the differences between the sexes in the action of selection.
3. We think that this definition is a long way from Darwin’s conception of sexual selection and sits more neatly alongside the current body of sexual conflict theory ( Parker 1979 ; Arnqvist and Rowe 2005 ).

As a definition of sexual selection – at least as usually envisaged – it is problematic as the sexes may experience different patterns of selection on traits unrelated to reproduction (that is ecological causes of sexual dimorphism, as discussed above: Shine 1989 ).

The corollary of this, as Carranza himself suggests, is that once we have separate sexual functions, then nearly all selection may be sexual selection. As such, sexual selection swallows natural selection (much as we saw natural selection swallowing sexual selection above). Therefore, whilst sexual selection may contribute to the opposing patterns of selection that arise on males and females (that is, sexual conflict), sexual conflict is most decidedly not the same thing as sexual selection ( Shuker 2010 ; Kokko et al.2014 ).

The final alternative definition of sexual selection we wish to consider explicitly is of a somewhat different nature: defining sexual selection in terms of one way in which it may be measured ( Shuster and Wade 2003 ; see suggestion in Roughgarden et al.2015 ).

Shuster and Wade (2003 ; henceforth S&W) summarized a research programme initiated by Wade and coworkers that sought to quantify the differences between males and females in the variance in the number of mates each sex obtained ( Wade 1979 ; Wade and Arnold 1980 ; Wade 1995 ). More formally, after Crow (1958, 1962 ), they show that the difference between males and females in the total opportunity of selection ( I males – I females ) is equal to what is termed I mates, where I represents the opportunity for selection.

S&W state that I mates gives a “standardized measure of the intensity of sexual selection on males and the sex difference in strength of selection” ( Shuster and Wade 2003, p.29). Importantly, as the authors also note, the opportunity for selection is just that, only the opportunity.

As such, I mates offers only an upper limit on selection. The I mates approach has been the subject of a number of critiques and rebuttals down the years (for example Sutherland 1985 ; Downhower et al.1987 ; Shuster and Wade 2003 ; Klug et al.2010 ; Krakauer et al.2011 ; Jennions et al.2012 ; Henshaw et al.2016 ).

We do not wish to rehearse that debate here. Rather we wish to argue against the use of this measure as a definition of sexual selection. First, it is true that one cannot measure what one cannot define. But to define something by its measurement is a different thing entirely, risking circularity and reification.
View complete answer

What is the principle underlying sexual selection and sexual conflict?

Notes –

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View complete answer

What is Darwin’s theory of sexual selection?

Sexual selection is Darwin’s second great insight, and he defined it as depending on ‘ the advantage which certain individuals have over other individuals of the same sex and species solely in respect of reproduction ‘. So sexual selection can be thought of as intra-specific reproductive competition.
View complete answer

What is the principle of Anisogamy Bateman?

Abstract – Males and females often display different behaviours and, in the context of reproduction, these behaviours are labelled sex roles. The Darwin–Bateman paradigm argues that the root of these differences is anisogamy (i.e., differences in size and/or function of gametes between the sexes) that leads to biased sexual selection, and sex differences in parental care and body size.

• This evolutionary cascade, however, is contentious since some of the underpinning assumptions have been questioned.
• Here we investigate the relationships between anisogamy, sexual size dimorphism, sex difference in parental care and intensity of sexual selection using phylogenetic comparative analyses of 64 species from a wide range of animal taxa.

The results question the first step of the Darwin–Bateman paradigm, as the extent of anisogamy does not appear to predict the intensity of sexual selection. The only significant predictor of sexual selection is the relative inputs of males and females into the care of offspring.
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What is parasite theory of sexual selection?

Discussion – We surveyed parasite infection of individuals in a wild salamander population across two years and demonstrate first that males have consistently higher trematode parasite loads than do females and second that parasite infection covaries negatively with tail height, a sexually selected trait in males.

Our results support the hypothesis that parasite infection may generally covary with the expression of sexual dimorphism and that the sexes may often differ in total parasite load; our results are also consistent with a fairly large body of work suggesting males may often carry higher parasite loads than females.

Sexual dimorphism in total parasite load can arise due to sex differences in resource allocation to immunocompetence or as a result of sexual differences in encounter rates with parasites. Although these pathways are often treated in the literature as separate agents of causality (e.g., Stoehr and Kokko 2006 ), we view them as tightly linked because sex differences in parasite encounter rates can arise, for example, due to differences between the sexes in time spent in different life stages, itself a component of the life history.

Although “immunocompetence” is itself a vague term, at some level it nonetheless represents an outcome of resource allocation to somatic maintenance. Thus, because parasite presence represents one cost determining the optimum time allocation to a life stage during ontogeny (e.g., Rowe and Ludwig 1991 ), parasite infection represents the total outcome of both time allocated to a life stage vulnerable to infection as well as resources allocated to immunocompetence and somatic maintenance, both of which may be shaped by selection in different ways for males and females.

In newts, males of some populations are more likely to overwinter in the aquatic stage, where they are vulnerable to parasite infection, than are females that often migrate out of ponds and overwinter on land (Grayson and Wilbur 2009 ; Grayson et al.2011 ).

1. However, sex differences in migration propensity do not appear to be present in the population of this study (De Lisle and Rowe 2014 ).
2. More importantly, parasites are probably rarely encountered in the winter because parasite loads reach their peak in the late spring/early summer (Raffel 2006 ).
3. However, females in several populations appear more likely to skip years of reproduction (Gill 1978 ; Grayson et al.2011 ) and thus exposure to the peak of parasite abundance, which may contribute to sex differences in parasite loads.

Finally, male and female newts differ in habitat use within ponds; males appear to spend more time in limnetic habitat, while females are more frequently found in the benthos (Grayson et al.2012 ). It is also possible that sex differences in immunocompetence play a role in the sex difference in parasite loads that we observed.

Although our data do not allow these alternatives to be distinguished, sexual dimorphisms in parasite load in newts and many other taxa (e.g., Reimchen and Nosil 2001 ) probably reflect a complicated outcome of divergences in life history, ecology, and immune investment. Relationships between trait expression and parasite load are often interpreted in light of models of parasite-mediated sexual selection, where female preference is maintained either via indirect genetic benefits sustained through host–parasite coevolution (Hamilton and Zuk 1982 ) or via direct selection to avoid parasites (Able 1996 ).

In newts, mating advantage for males with tall tails appears to arise from scramble competition among males for access to mating opportunities (Verrell 1983 ; Able 1999 ) rather than female preference (Gabor et al.2000 ), and the complex life cycle of Clinostomum precludes transmittance between parents and offspring.

Thus, our results support the hypothesis that parasite infection may often covary with expression of sexually selected traits even if parasites play no major role in the maintenance of female preference. We found evidence for a weak relationship between female parasite load and tail size, suggesting a similar but weaker pattern to that found in males.

In many organisms, some sexually selected male traits are not completely sex-limited in expression, in that an analogous female trait may be expressed at or closer to the optimum favored by natural selection as is the case with newt tail height. Few studies examine the relationship between the expression of female analogs of sexually selected traits and female parasite loads.

Such a relationship may suggest the presence of intralocus sexual conflict over the reaction norm of the trait, if the evolution of condition-dependent expression in males also leads to an increase in condition-dependent expression in females (Bonduriansky and Rowe 2005 ). Such a relationship could also suggest intralocus conflict over immune investment, if the optimal relationship between condition and immune investment differs between the sexes.

Both genetic conflicts could affect the net fitness effect of mating bias for females (Gorton 2012 ; Long et al.2012 ). In fact, sexual dimorphism in optimal immunocompetence generated by sexual selection (Stoehr and Kokko 2006 ) could generally lead to intralocus sexual conflict over optimal immune investment, eliminating any “good-genes” effects of female preference as envisioned by Hamilton and Zuk ( 1982 ) and others since (Møller and Alatalo 1999 ; Møller et al.1999 ).

Our work illustrates that parasite infection may be generally related to sexual dimorphism within species. Further, hypotheses of parasite-mediated sexual selection predict a positive relationship between parasite load and sexual dimorphism among species (Hamilton and Zuk 1982 ). Yet this pattern too has a more parsimonious explanation, suggested originally by George Williams (Williams 1966a, b ; Partridge and Endler 1987 ); sexually selected traits are part of the reproductive effort and should covary with life history and thus optimal investment in somatic maintenance (immunity), among species.

That is, for species with low residual reproductive value, selection would favor increased allocation to current reproductive effort (including sexually selected traits in males) and reduced allocation to maintenance of the soma (including immune investment); the opposite would be true for taxa with high residual reproductive value.

Thus, the most readily testable predictions of hypotheses of parasite-mediated sexual selection have immediate alternative explanations, which underscores Balenger and Zuk’s ( 2014 ) emphasis that tests of parasite-mediated sexual selection should instead focus on the dynamics of host–parasite coevolution.

Although parasites do represent a cost that may influence the evolution of life histories, including the expression of male reproductive effort, relationships between dimorphism and parasite load within and among species do not necessarily imply a direct role for host–parasite coevolution in mediating sexual selection.
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