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Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration.

Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait the mandibleswhile also testing for effects on female lifetime reproductive success.

We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes—the indirect effect on females—when natural selection targets sex-limited sexually selected characters.

Sexual selection typically acts more strongly on males and is responsible for the evolution of a vast array of exaggerated characters that enhance male sexual fitness components 1234. They also demonstrate how natural selection can oppose sexual selection as trait values move beyond their naturally selected optima reviewed in ref. While theory is clear on the t effects of natural and sexual selection on sexual trait evolution, explicit experimental tests of theoretical predictions are required to fully understand sexual trait evolution One potentially important source of natural selection that could affect the evolution of sexually selected traits is predation 1and many studies have shown predation can seemingly oppose the exaggeration of male sexual characters.

For example, sexual als are conspicuous to potential mates but may also attract predators and parasitoid This is particularly well documented in orthopterans and frogs 12131415161718and this form of natural selection is probably responsible for the loss of cricket sexual als on two Hawaiian islands 19 More generally, predation appears to reverse the evolution of extreme sexually selected phenotypes reviewed in the ref. Nonetheless, while there is ample evidence that predation selects against sexual trait enhancement, there is limited direct experimental verification that this selection causes evolutionary responses in these traits but see e.

Female reproductive success can also be impacted by predation 28 For example, egg-carrying females can be slower 3031 and suffer higher predation rates 29 Resultant anti-predator behaviors may reduce foraging efficiency and reproductive activity, and thus be costly to females reviewed in the ref.

Costs can accrue via delayed development, slower growth or postponed reproduction 333435 Nonetheless, while there is ample evidence that predation selects on both females and males, the t action of selection on the sexes is frequently investigated independently.

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Unfortunately, without exploring how predation affects both sexes, we are unlikely to fully understand how predation affects sexual trait evolution This is especially true when intersexual genetic correlations link sexually selected male characters with female fitness, because selection on one sex can affect the other through these correlations 37 And again, controlled experimental tests for evolutionary responses to predation are usually not undertaken.

Here, we use the broad-horned flour beetle Gnatocerus cornutus to directly test for effects of predation on the evolution of a male sexually selected character their mandibles and female lifetime reproductive success LRS. The enormously enlarged male mandibles are used in male—male fights, and males with larger mandibles have higher fighting and mating success 394041 Females lack this exaggerated character completely 40 work has shown that males with larger mandibles sire daughters with lower fecundity, and that directly selecting for increased or decreased mandible size in decreased or increased female fitness LRS 40 Basically, the enlarged male mandible requires a masculinized head and prothorax to function optimally and this means males with larger mandibles have smaller abdomens 40 Thus although females never develop mandibles, selecting on male mandibles ultimately affects female abdomen size, which likely determines the of eggs a female carries 40 These G.

The assassin bug Amphibolus venatorwhich preys on various stored-product insect pests including flour beetles 48is the model predator. After eight generations of experimental evolution, we measure female fitness LRS and a range of morphological characters, including mandible size. Morphology was also measured during experimental evolution. We find strong effects of male-specific predation on morphology and female fitness, while predation on females alone had no effects. We additionally test for associations between male mandible size and predation likelihood and find larger mandibles result in greater likelihood of predation, and also show that evolving under predation made males less effective fighters.

The genetic parameters estimated from the animal model analyses confirmed what experimental evolution studies had only inferred 39 Likelihood ratio comparisons of univariate models confirmed the presence of additive genetic variance in all four traits Supplementary Tables 1 — 2 as expected. Parameter estimates from the full multivariate model show substantial genetic variation in all traits measured and reasonably high trait heritability Table 1.

All traits were positively genetically correlated except male mandible size and female fitness lifetime reproductive success and male mandible size and abdominal mass, which were both strongly negatively correlation. The lack of correlation between body and abdomen mass is consistent with findings The experimental treatments we imposed on the replicated beetle populations generated treatment specific evolutionary responses in some traits but not others, and responses were not linear Fig.

When we compared trait values at the end of the experimental evolution period, we found that male predation ificantly reduced male mandible size Fig. Total male body size was unaffected by our treatments Fig. Shown are male mandible size mm amale abdomen size mg bmale body size mg cfemale abdomen size mg d and female body size mg e population means. Black circles are the control populations that were not subjected to selection by predation.

Blue squares and red triangles, are the populations with male and female exposure to predators, respectively. Note we did not measure female fitness lifetime reproductive success: LRS at every generation as it was not logistically possible.

Source data are provided as a Source Data file. Traits were: Male mandible size mm aMale abdomen size mg bMale body size mg cFemale lifetime reproductive success LRS: offspring dFemale abdomen size mg eand Female body size mg f shown are upper and lower quartile the box with medians lines and each dot represents the mean of one replicate population.

Only populations evolve and thus population is the biologically relevant unit of replication in an experimental evolution study. Predation also affected female LRS Fig. Thus exposing males to predators resulted in the evolution of smaller male mandibles and higher female fitness. As with males, female abdomen size also increased under male predation Fig.

Finally, female body size was unaffected by our experimental regimes Fig. In the direct assessment of associations between mandible size and predation probability, 45 of 70 male G. The likelihood of being attacked by the predator was positively associated with mandible size Fig.

Possible reasons for this are discussed below. The graph shows that as mandible size increases so does the likelihood of predation. The curve is the fitted frequency from the GLM with dot size representing s 1—6 of individual G. Inset shows an A. Note the size difference. To summarize the main findings: male-specific predation in the evolution of an altered, more feminized male phenotype that includes reductions in the size of a male-limited sexually selected trait. The upper panel is a diagrammatic representation of the male and female phenotypes resulting from male-limited predation in comparison to those resulting from sexual selection on males.

Sexual selection left images in enlarged male mandibles, which require a masculinized head and prothorax to operate effectively. This fore-body masculinization in a smaller male abdomen and because of intersexual correlations for abdomen size, a smaller female abdomen and capacity for fewer eggs, even though females never develop mandibles. Male-limited predation selects against the masculinized phenotype, ultimately resulting in larger male and female abdomens, and hence more eggs and higher fitness females images on the right.

The lower plate shows beetles from the male predation and control treatments and reveals the impact of evolving with male predation described above—both males and female evolve more feminized phenotypes smaller mandibles for males and larger abdomen for both compared to the controls NB controls and female-predation have similar phenotypes Figs.

Images were created by us. Predation is frequently invoked as an evolutionary brake on the exaggeration of sexually selected traits and there are many studies consistent with this logic, usually documenting selection against larger characters or assessing macro-evolutionary patterns consistent with it 26 Here, we employ experimental evolution and directly demonstrate that male-specific predation not only reversed the exaggeration of a sexually selected trait, but additionally, this reversal in higher female fitness.

This boost to female fitness occurs because predators select against larger mandibles, and this in a less masculinized beetle phenotype including a larger abdomenand because of shared genetic architecture across the sexes, females also become more feminized and produce more offspring. We discuss these findings in turn. The likelihood of predation increases with male mandible size and when populations were forced to evolve with predation on males, smaller mandibles evolve. Thus increased natural selection via predation reduces the size of a sexually selected trait, which is broadly consistent with theory 56 reviewed in the ref.

work with G. Mandible size is negatively phenotypically and genetically associated with locomotor activity 49and locomotor activity running is a predator escape mechanism in flour beetles Reduced running and lower escape rates for males with large mandibles would explain the microevolutionary pattern we detect. Interestingly, there is no intersexual correlation for locomotion in this beetle 49so there was no expectation that predation on females should impact male running speed and hence morphology.

Be that as it may, we clearly show that predation risk increases with mandible size and that this natural selection reverses the evolutionary exaggeration of a sexually selected male trait. Females from the male-predation populations evolve higher fitness higher LRS when mating with stock tester males even though females were not directly exposed to predators.

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ly Harano et al. This occurred because selection for increased mandible size resulted in a more masculinized phenotype, and Harano et al.

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The intersexual genetic associations we document here, especially the negative male mandible-female LRS correlation, flesh out this explanation and confirm inference Negative intersexual fitness associations are common 5152 because alleles conferring high fitness to one sex frequently lower fitness in the other 53 In addition to any sexually antagonistic selection on body morphology, male beetles with larger mandibles are also more aggressive toward females Thus exposure to males with larger mandibles potentially reduces female LRS due to misdirected male attacks Therefore, there could be two avenues to increased female fitness when predators select against large male mandibles, a reduction in ontogenetic conflict load intralocus sexual conflict load 37and reduced male-to-female aggression.

In any case, predation on males causes an evolutionary reduction in mandible size and this in higher female fitness. Thus male-biased predation indirectly selects for an increase in female quality, which is an interesting outcome. The net population level effects of sexual selection and sexual conflict over optimal phenotypes are not clear 5156with for example, evidence that sexual selection can both increase and decrease population extinction rates 5758 Additionally, intralocus sexual conflict as documented in the flour beetle 40 is thought to constrain population adaptation because sexually antagonistic selection keeps each sex from its fitness optima 51 Our suggest that predator removal of males with the largest sexual traits reduces intralocus ontogenetic sexual conflict costs, enhancing female reproductive performance, which should all else being equal increase population productivity.

Relaxing other sexual conflict can also increase population fitness 61 As we show, sex-biased predation can have analogous indirect effects intra-specifically predation on males increases female fitness. However, the indirect impacts we document are unidirectional since female-biased predation does not alter female fitness or male sexual-trait size. Micro-evolutionary responses to our treatments were not readily apparent until about four or five generations of selection, after which there was clear treatment-specific divergence.

Non-linear responses like this are common in selection studies 6566 and see e. This includes genetic asymmetries i. We have no way of knowing the mechanistic cause of the patterns we document, but note that responses to directly selecting on mandible size ly revealed similar non-linearity There have also been many studies showing that males with smaller mandibles are less competitive and have lower fitness 3940and that fighting ability is genetically correlated with mandible size Consistent with these findings, males evolving with male-predation have smaller mandibles and are less adept fighters.

Overall this study provides direct evidence that predator-mediated natural selection can evolutionarily reverse the exaggeration of a sexually selected trait. This finding is consistent with a vast body of fundamental theory 5669 and empirical evidence from observational and correlational studies 19 reviewed in the ref.

We also reveal interesting outcomes when natural selection targets sex-limited sexually selected characters, since predator removal of a male-imposed conflict load increases female fitness. Thus sex-biased predation within a species can essentially mimic indirect ecological competition effects, as discussed above. Investigating the precise mechanistic detail and population level fitness effects of some of these findings is now required. The G. This beetle is a stored product pest, and thus the laboratory conditions very closely mimic what have become their natural conditions.

Virgin males and females were removed from the stock population as final instar larvae. Each larva was placed in one well of a well tissue culture plate Cellstar; Greiner Bio-One, Frickenhausen, Germany until adult eclosion because pupation in G. After eclosion, both sexes were allowed to sexually mature for a period of 14 days prior to their use.

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