Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles

Sexual selection is thought to favor the evolution of secondary sexual traits in males that contribute to mating success. In species where females mate with more than one male, sexual selection also continues after copulation in the form of sperm competition and cryptic female choice. Theory suggests that sperm competition should favor traits such as testes size and sperm production that increase a male's competitive fertilization success. Studies of experimental evolution offer a powerful approach for assessing evolutionary responses to variation in sexual selection pressures. Here we removed sexual selection by enforcing monogamy on replicate lines of a naturally polygamous horned beetle, Onthophagus taurus, and monitoring male investment in their testes for 21 generations. Testes size decreased in monogamous lines relative to lines in which sexual selection was allowed to continue. Differences in testes size were dependent on selection history and not breeding regime. Males from polygamous lines also had a competitive fertilization advantage when in sperm competition with males from monogamous lines. Females from polygamous lines produced sons in better condition, and those from monogamous lines increased their sons condition by mating polygamously. Rather than being costly for females, multiple mating appears to provide females with direct and/or indirect benefits. Neither body size nor horn size diverged between our monogamous and polygamous lines. Our data show that sperm competition does drive the evolution of testes size in onthophagine beetles, and provide general support for sperm competition theory.     

Female choice, male interference, and sperm precedence in the red-spotted newt

Darwin first identified female choice and male—male competitionas forms of sexual selection resulting in the evolution of conspicuoussexual dimorphism, but it has proven challenging to separatetheir effects. Their effects on sexual selection become evenmore complicated when sperm competition occurs because spermprecedence may be either a form of cryptic female choice ora form of male—male competition. We examined the effectsof tail height on male—male competition and female choiceusing the sexually dimorphic red-spotted newt (Notophthalmusviridescens viridescens). Experiment 1 examined whether maletail height influenced male mating success. Males with deeptails were more successful at mating with females than thosewith shallow tails. Successful, deep-tailed males also were bigger(snout-vent length; SVL) than unsuccessful, shallow-tailed males,but they did not vary in tail length or body condition. Of these,only tail height and tail length are sexually dimorphic traits.Experiment 2 tested the hypothesis that the differential successof males with deeper tails was due to female choice by examiningboth simultaneous female preference for association and sequentialfemale choice. We found no evidence of female choice. When maleswere not competing to mate with females, tail height did notinfluence male mating success. Successful males did not havedifferent SVL and tail lengths than unsuccessful males. Thus,tail height in male red-spotted newts appears to be an intrasexuallyselected secondary sexual characteristic. Experiment 3 usedpaternity exclusion analyses based on molecular genetic markersto examine the effect of sperm precedence on sperm competitionin doubly-mated females. Sperm precedence likely does not havea pervasive and consistent effect on fertilization success becausewe found evidence of first, last, and mixed sperm usage.     

The unexpected but understandable dynamics of mating,paternity and paternal care in the ocellated wrasse

Although theory generally predicts that males should reduce paternal care in response to cues that predict increased sperm competition and decreased paternity, empirical patterns are equivocal. Some studies have found the predicted decrease in male care with increased sperm competition, while even more studies report no effect of paternity or sperm competition on male care. Here, we report the first example, to our knowledge, of paternal care increasing with the risk and intensity of sperm competition, in the ocellated wrasse (Symphodus ocellatus). Theory also predicts that if paternal care varies and is important to female fitness, female choice among males and male indicators traits of expected paternal care should evolve. Despite a non-random distribution of mating success among nests, we found no evidence for female choice among parental males. Finally, we document the highest published levels of extra-pair paternity for a species with exclusive and obligate male care: genetic paternity analyses revealed cuckoldry at 100 per cent of nests and 28 per cent of all offspring were not sired by the male caring for them. While not predicted by any existing theory, these unexpected reproductive patterns become understandable if we consider how male and female mating and parental care interact simultaneously in this and probably many other species.     

Evolution under relaxed sexual conflict in the bulb mite Rhizoglyphus robini

The experimental evolution under different levels of sexual conflict have been used to demonstrate antagonistic coevolution in muscids, but among other taxa a similar approach has not been employed. Here, we describe the results of 37 generations of evolution under either experimentally enforced monogamy or polygamy in the bulb mite Rhizoglyphus robini. Three replicates were maintained for each treatment. Monogamy makes male and female interests congruent; thus selection is expected to decrease harmfulness of males to their partners. Our results were consistent with this prediction in that females from monogamous lines achieved lower fecundity when housed with males from polygamous lines. Fecundity of polygamous females was not affected by mating system under which their partners evolved, which suggests that they were more resistant to male-induced harm. As predicted by the antagonistic coevolution hypothesis, the decrease in harmfulness of monogamous males was accompanied by a decline in reproductive competitiveness. In contrast, female fecundity and embryonic viability, which were not expected to be correlated with male harmfulness, did not differ between monogamous and polygamous lines. None of the fitness components assayed differed between individuals obtained from crosses between parents from the same line and those obtained from crosses between parents from different lines within the same mating system. This indicates that inbreeding depression did not confound our results. However, interpretation of our results is complicated by the fact that both males and females from monogamous lines evolved smaller body size compared to individuals from polygamous lines. Although a decrease in reproductive performance of males from monogamous lines was still significant when body size was taken into account, we were not able to separate the effects of male body size and mating system in their influence on fecundity of their female partners.     

A theoretical study on the evolution of male parental care and female multiple mating: effects of female mate choice and male care bias

Male parental care and female multiple mating are seen in many species in spite of the cost they entail. Moreover, they even coexist in some species though polyandry, by reducing paternity confidence of caregiving males, seems to hinder the evolution of paternal care. Previous studies have investigated the coevolutionary process of paternal care and polyandry under various simplifying assumptions, including random mating and random provision of male care. We extend these models to examine possible effects of female mate choice and male care bias, assuming that (a) monandrous females mate preferentially with caregiving males while polyandrous females compromise their preference in order to mate with multiple males and (b) caregiving males tend to direct their care to offspring of monandrous females. Our models suggest that both the female preference and the male bias always favor caregiving males while they may not always facilitate the evolution of monandry.     

Experimental evidence that female ornamentation increases the acquisition of sperm and signals fecundity

Mate choice can lead to the evolution of sexual ornamentation. This idea rests on the assumption that individuals with more elaborate ornaments than competitors have higher reproductive success due to gaining greater control over mating decisions and resources provided by partners. Nevertheless, how the resources and quality of sexual partners that individuals gain access to are influenced by the ornamentation of rival individuals remains unclear. By experimentally concealing and subsequently revealing female ornaments to males, we confirm in the fowl, Gallus gallus, that female ornamentation influences male mating decisions. We further show, by manipulating the relative ornament size of females, that when females had larger ornaments than competitors they were more often preferred by males and obtained more sperm, especially from higher quality males, as measured by social status. Males may benefit by investing more sperm in females with larger ornaments as they were in better condition and produced heavier eggs. Female ornament size also decreased during incubation, providing a cue for males to avoid sexually unreceptive females. This study reveals how inter-sexual selection can lead to the evolution of female ornaments and highlights how the reproductive benefits gained from mate choice and bearing ornaments can be dependent upon social context.     

Body Weight and Rearing Conditions of Males, Female Choice and Paternities in a Small Mammal, Cavia aperea

Patterns of mate choice may be important determinants of a species' social organisation and mating system. At least two different aspects of female mate choice can be distinguished: choice of a social partner and choice of the genetic father of the offspring. Different characteristics of males can qualify them for these two roles. Although social and reproductive partners have been shown to differ in many species, social association times are often used in laboratory choice tests to infer reproductive preferences. The traits for which females may choose partners are diverse. Body size can correlate with the male's strength in defending resources or other abilities benefiting the female and her offspring. In species living in social groups, social skills learned from group members during infancy can be important for later reproductive success. In this laboratory study, we conducted choice tests with wild cavies, Cavia aperea , a harem-living species of South American rodents, to determine social preferences of females towards two simultaneously available males. For offspring sired during these tests, paternities were determined by microsatellite DNA profiling. Males used in the tests differed in body weight and in rearing conditions: Half of the males had been reared in the presence or absence of their father, respectively. Male rearing conditions had no effect on either female social preferences or paternities. Females significantly preferred heavier males as social partners. In five of six tests, the heavier male also sired the offspring. Sires were in most cases but not consistently socially preferred. Heavier males may be preferable as social partners because they are better able to provide females with resources or have more experience in paternal care or predator avoidance as weight correlates with age. When choosing reproductive partners, females may prefer other male traits and the distribution of paternities may also be influenced by sperm competition.     

The male and female perspective in the link between male infant care and mating behaviour in Barbary macaques

Infant care from adult males is unexpected in species with high paternity uncertainty. Still, males of several polygynandrous primates engage in frequent affiliative interactions with infants. Two non‐exclusive hypotheses link male infant care to male mating strategies. The paternal investment hypothesis views infant care as a male strategy to maximize the survival of sired offspring, while the mating effort hypothesis predicts that females reward males who cared for their infant by preferably mating with them. Both hypotheses predict a positive relationship between infant care and matings with a particular female. However, the paternal investment hypothesis predicts that increased matings come before infant care whereas the mating effort hypothesis predicts that infant care precedes an increase in matings. Both hypotheses are usually tested from the perspective of the proportion of matings and care that individual females engage in and receive, rather than from the perspective of the care and mating behaviour of individual males. We tested the relationships between care and mating from both female and male perspectives in Barbary macaques. Mating predicted subsequent care and care predicted subsequent mating when viewed from the male but not the female perspective. Males mainly cared for infants of their main mating partners, but infants were not mainly cared for by their likely father. Males mated more with the mothers of their favourite infants, but females did not mate more with the main caretakers of their infants. We suggest that females do not choose their mating partners based on previous infant care, increasing paternity confusion. Males might try to increase paternal investment by distributing the care according to their own instead of female mating history. Further, males pursue females for mating opportunities based on previous care.     

Female egg dumping and the effect of sex ratio on male egg carrying in a coreid bug

Phyllomorpha laciniata Vill (Heteroptera, Coreidae) is uniqueamong terrestrial insects in that females glue eggs on the backsof other conspecifics. Egg carrying byP. laciniatamales haspreviously been considered as paternal care. We explored femaleoviposition with respect to previous mating experience of femalesand tested whether sex ratio affects male egg-carrying. Thehypothesis that male egg-carrying is a form of paternal carepredicts that a male should always accept eggs after matingwith a female. However, if male egg-carrying is a form of postcopulatorymate guarding rather than paternal care, egg carrying shouldincrease in the presence of other males. When two couples wereplaced together, females laid eggs on the backs of all individualsenclosed, including the backs of other females. However, whena female was accompanied by 2 males, 22 out of 26 females ovipositedon their mating partner. Thus, sexual competition rather thanpaternity alone, affects a male's eagerness to carry eggs. However,even if males sometimes carry their own eggs, females lay eggson the backs of all conspecifics they can easily acquire. Thus,egg carrying in P. laciniata is partially voluntary and partiallythe result of female egg dumping     

Influences of sex, size, and symmetry on ejaculate expenditure in a moth

Although sperm fundamentally function to fertilize eggs, forcesarising from both sexes select for optimal ejaculate composition.Sperm competition is one recognized agent in the evolution ofsperm and ejaculate structure. Few studies, however, have examinedhow female factors influence ejaculate structure, despite somebehavioral evidence for male mate choice. Male Plodia interpunctella(Lepidoptera, Pyralidae) accrue all resources for reproductionas larvae. Adults emerge with a limited sperm complement andare therefore under intense selection to optimize gamete allocation.I detected no effect of male body weight on ejaculate size.However, female reproductive potential (ovary masses) was dictatedby body weight In addition, heavier females had greater spermathecalvolumes, but there was no such relationship with bursal size.Finally, heavier females showed a higher mating frequency. Ifound that mating males were sensitive to female size and producedlarger ejaculates when mating with heavier females. Males mayejaculate more sperm into larger females either because it paysthem to "spend" more reproductive resources on matings thatprovide greater reproductive potential, or because heavier (longerlived and more attractive) females mate more frequently andhave larger spermathecal volumes. Alternatively, females maycontrol spermatophore formation and "accept" an appropriateejaculate to maximize fertility. Males may therefore be alsoselected to ejaculate more sperm into larger females to counteractgreater risks of sperm competition associated with heavier females.There was no association between male or female femur asymmetryand ejaculate size. P.interpunctella may be selected to exercisemodulation of ejaculate size because males invest paternally,sperm for the single reproductive episode are limited, and femalefecundity and mating pattern vary between individuals and areassociated with body weight. More obvious variability in malereproductive behavior and choice may therefore be paralleledat the cryptic gametic level by plasticity in ejaculate allocation.     

The importance of sperm competition risk and nest appearance for male behavior and female choice in the sand goby, Pomatoschistus minutus

To test if an increased sperm competition risk affects malebehavior and mating decisions of both sexes, we performed twoexperiments using the sand goby, Pomatoschistus minutus, a nest-buildingfish with exclusive paternal care. In our first experiment,a nest-holding male, with a confined female, was sequentiallyexposed to a vial with a sneaker male or an empty vial. Whilemale courtship, nest building, displacement fanning, and timeoutside the nest were unaffected, individual males showed ahigher mucus preparation effort inside the nest in the presenceof a sneaker male than when alone. We found such mucus to containsperm, thus clearly suggesting an importance in sperm competition.In our second experiment, a female was free to spawn with twodifferent males, one of which was exposed to a confined sneakermale. Male mating success was not affected by the presence ofa sneaker male. However, the volume of sand the male had puton his nest was positively associated with female spawning decision,while nest-opening width was not. In a partial correlation offive traits thought to attract females (nest-opening width,sand volume, male courtship display, displacement fanning, andmale size), males that fanned well were found to also buildlarge nests or display intensely, but not both. This indicatesthat rather than being jacks-of-all-trades, individual malesfocus on a subset of traits for attracting females.     

Alternative Female Choice Tactics in the Scorpionfly Hylobittacus apicalis(Mecoptera) and Their Implications

Females of the scorpionfly Hylobittacus apicalis choose mateson the basis of material benefits (nuptial arthropod prey size)and probably on the basis of genetic benefits males deliverat mating. Females feed on the male's prey throughout copulation.They prefer males with large prey as mates and often refusemales who present small prey. That females may value male geneticquality is suggested by differences in ability of males to obtainlarge prey, which if inherited would influence offspring fitness,and by females often terminating mating with males with smallprey before they transfer any sperm or a complete ejaculate.Females hunt only when males with prey are not available becausehunting exposes individuals to predators. Female Hylobittacusapicalis exhibit alternative mate choice tactics, which arecondition-dependent in expression and probably comprise a conditionalstrategy. Body size, recent feeding history, and male availabilitydetermine how discriminating an individual female actually is,and these conditions may determine the value of material andgenetic benefits in mate choice decisions. The results suggestthat female choice controls male behavior. When females becomechoosy, males are forced to obtain rare large prey despite theincreased risks to males associated with this behavior. The implications of the findings on H. apicalis are discussedin relation to condition dependent female choice patterns inother species and the evolutionary maintenance of female choice.     

Females prefer mating males in the carmine triplefin,Axoclinus carminalis,a paternal brood-guarder

Synopsis This study investigates the role of male mating status in female choice patterns in the carmine triplefin, Axoclinus carminalis, a tripterygiid fish that exhibits paternal care. The distribution of daily reproductive activity is clumped, with many males receiving no mates and some receiving three or more. Females in this species do not prefer larger males, and characteristics of the oviposition site appear to have minimal effects on male mating success. When a female is removed from a male early in the daily spawning period, that male attracts fewer additional females for the remainder of the spawning period than does a control male. These changes in mating success are temporary, and do not affect mating success on subsequent days. A preference for mating males or males that are guarding eggs could provide asymmetric benefits for males to defend oviposition sites. This preference for males with eggs could be acting alone or with other factors such as high variance in oviposition site quality to favor the evolution of paternal care in fishes.     

Female ornamentation, parental quality, and competitive ability in the rock sparrow

The evolution of female ornaments is poorly understood. Recent evidence suggests not only that female ornaments may be genetic correlates of selection on males but may also have evolved through male mate choice and/or through female–female aggressive interactions. In the rock sparrow, Petronia petronia, both sexes have a carotenoid-based yellow patch that is sexually selected by both sexes. The benefits that male may gain from choosing an attractive female remain unidentified. Both parents participate in caring for the young, so there should be mutual mate choice because males and females should both benefit from choosing a good parent (good parent hypothesis; GPH). Moreover, it has already been demonstrated that the yellow patch in males is also a badge of status (armament). Therefore, the yellow patch could also serve as both ornament and armament in females (dual utility hypothesis; DUH). We investigated the hypothesis that male and female yellow patch size signals parental quality in the field. We tested by an experiment in captivity the signal function of the yellow patch in female–female aggressive interactions for access to food. Yellow patch size correlated with paternal, but not maternal, feeding rates. Thus, this study supports the hypothesis that yellow patch dimension signals male parental quality, but there is no evidence for the GPH to explain female ornamentation. In the experiment females with relatively large yellow patches had earlier access to food than those with small patches. These results seem to suggest that a sexually selected carotenoid-feather signal may be used in female–female competition, in agreement with the DUH. Males may benefit from choosing well ornamented females because these may be superior competitors.     

Enhanced vigilance in monogamous pairs of the lizard, Tiliqua rugosa

The Australian sleepy lizard, Tiliqua rugosa, forms monogamouspairs for up to 8 weeks each spring before mating. We observedthat males had food in their mouths significantly less oftenwhen they were in pain than when they were alone. Females hadfood in the mouth independent of the presence or absence ofmales. Among females that had been feeding, indicated by foodin the mouth, we observed them feeding, as we approached, lessoften when they were in pairs than when they were alone. Amongfemales in pairs with food in their mouths, we observed themfeeding less often when their male partners were not feedingthan when their partners were feeding. This suggests that femalesare alerted to approaching danger earlier when they are in apair, and alerted earlier in a pair when their male partneris not feeding. Enhanced vigilance may be one function of pairingbehavior.     

Is male plumage reflectance correlated with paternal care in bluethroats?

Although it is now well established that the conspicuous maleplumage colors of many birds have been subject to sexual selectionby female choice, it is still debated whether females matewith colorful males to obtain direct or indirect benefits.In species where males provide substantial parental care, femalesmay obtain direct benefits from mating with the males that are best at providing care. The good parent hypothesis suggeststhat male plumage coloration signals a male's ability to provideparental care. Alternatively, the differential-allocation hypothesissuggests that colorful males reduce their care in responseto increased investment by females mated to attractive males.We tested these hypotheses on the bluethroat (Luscinia s. svecica),a socially monogamous, sexually dichromatic bird, in which males have a colorful throat patch consisting of a structurallyderived blue area surrounding a melanin-based chestnut spot.Male plumage coloration was objectively quantified by use ofreflectance spectrometry. We found no evidence of a relationshipbetween male coloration of either the blue patch or the chestnutspot and the level of paternal care. Nor were there any correlationsbetween male coloration and body size or body condition. Thus, our study does not support the hypothesis that male colorationsignals male parental quality (the good parent hypothesis)or the hypothesis that colorful males reduce their care inresponse to increased investment by females (the differential-allocationhypothesis).     

Mate Quality and Novelty Influence Post‐Copulatory Female Choice in Decorated Crickets,Gryllodes sigillatus

Females of many taxa prefer to mate with novel males rather than previous mates, but also favor males that have traits indicative of higher genetic quality or compatibility. However, it may not be possible for females to simultaneously choose males that are both novel and of high quality, and the female response to this dilemma has not previously been examined. In this paper, we ask whether female decorated crickets, Gryllodes sigillatus, exert their choice for novel males via post‐copulatory choice (sperm ampulla removal) and whether male genetic background (variation in male quality) affects this decision. We found that after matings with inbred males, females removed the ampullae of familiar mates sooner than those of novel males, whereas after matings with outbred males, there was no difference in the ampulla‐retention times of familiar mates and novel partners. This suggests that when male do not vary in quality, females prefer novel partners. However, when males vary in quality, female preferences for male traits are more important than preferences for novel partners.     

Male Mating History Influences Female Mate Choice in the Trinidadian Guppy (Poecilia reticulata)

Based on the phenotype‐linked fertility hypothesis, sexual selection should favour females that can accurately assess the recent mating history of available sexual partners and preferentially avoid mating with recently‐mated males [who may be sperm depleted (SD)] so as to minimize the risk of their eggs not being fertilized. This hypothesis has received to date only limited attention and empirical support. Therefore, in the current study, we investigated experimentally whether females of a vertebrate species, the Trinidadian guppy (Poecilia reticulata), are able to assess the recent mating history of males, and thus potentially their functional fertility, and choose to avoid mating with males that appear to have recently mated and who may be sperm limited. Individual virgin females were first given a dichotomous choice between a male that had not been recently observed to interact sexually with another female (i.e. not sperm‐depleted) and another male that had been observed to interact sexually with a female (i.e. potentially sperm‐depleted) as sexual partners. Paired males were matched for body length and coloration. Immediately following this test, the focal females were subjected to a free‐swimming mate‐choice test using the same paired stimulus males. As predicted, on average, female guppies avoided the apparently recently‐mated (and potentially sperm‐depleted) male and exhibited a significant preference for the other male not recently observed mating (and thus not likely sperm limited) during both tests. We do not yet fully understand the underlying mechanisms of this preference. Therefore, further research on the particular cues that females use to assess the recent mating history and fertility status of males is required.     

Female macaques compete for ‘power’ and ‘commitment’ in their male partners

The formation of male-female social bonds and the resulting competition among females for male partners is a core element of human societies. While female competition for a male partner outside the mating context is well studied in humans, evidence from non-human primates is scarce, and its evolutionary roots remain to be explored. We studied two multi male – multi female groups of wild Assamese macaques (Macaca assamensis), a species where females gain benefits from selectively affiliating with particular males. Using a behavioral data set collected over several years, we tested whether females competed over access to male social partners, whether success in competition was driven by female dominance rank, and which male traits were most attractive for females. We found assortative bonding by dominance rank between females and males, which together with females initiating and maintaining contact suggests direct female competition over males. Two male traits independently predicted male attractiveness to females: (1) current dominance rank, a measure of 'power' or a male's ability to provide access to resources, and (2) prior male affiliation with immatures, a measure of a male's potential paternal proclivity or 'commitment' to infant care. Both traits have been consistently identified as drivers of female partner choice in humans. Our study adds to the evidence that female competition for valuable male partners is not unique to humans, suggesting deep evolutionary origins of women's mate choice tendencies for ‘power’ and ‘commitment’.     

Mating strategies based on foraging ability: an experiment with grasshoppers

Female mate choice and the benefits of this behavior are criticalaspects of Darwinian sexual selection, but they are seldom documentedbecause it is difficult to identify the male trait(s) that femalesmay be seeking. We conducted experiments with grasshoppers (Melanoplussangutnipes: Orthoptera, Acrididae) to examine this behavior.Males that feed more intensively and select a diet mix thatpermits greater food intake (food intake per body mass per time)in laboratory trials were preferentially selected by females.These better foraging males on average provide greater paternalinvestment (greater spermatophore mass) to the female, whichincreases her reproductive rate (eggs produced per body massper time). However, paternal investment may not entirely explainfemale choice of better foraging males, because these maleswere still selected even if they had their food intake restrictedor had been allowed to recently mate, which reduces spermatophoreproduction. Furthermore, males change their mating strategyin response to female choice and the foraging abilities of surroundingmales. Poorer foraging males attempt forcible copulation ratherthan displaying and allowing female choice. A male will facultativelyswitch between these strategies depending on the foraging abilitiesof the surrounding males. While females attempt to reject forciblecopulation, forcible copulation reduces the frequency with whichfemales successfully copulate with better foraging males. Therefore,males that are less "attractive" to females adopt alternativemating strategies to counter female choice which would excludethem from mating.[Behav Ecol 7: 438–444 (1996)]