Indiscriminate females and choosy males: within- and between-species variation in Drosophila

Abstract The classic view of choosy, passive females and indiscriminate, competitive males gained theoretical foundations with parental investment theory. When females invest more in offspring than males, parental investment theory says that selection operates so that females discriminate among males for mates (i.e., females are choosy and passive) and males are indiscriminate (i.e., males are profligate and competitive). Here we report tests of predictions using Drosophila pseudoobscura and D. melanogaster , with typical asymmetry in gamete sizes (females > males), and in D. hydei with far less asymmetry in gamete size. Experimental observations revealed that the labels "choosy, passive females" and "profligate, indiscriminate males" did not capture the variation within and between species in premating behavior. In each of the species some females were as active in approaching males (or more so) than males in approaching females, and some males were as discriminating (or more so) than females. In pairs focal males and females responded differently to opposite-sex than to same-sex conspecifics. Drosophila hydei were less sex-role stereotyped than the other two species consistent with parental investment theory. However, D. pseudoobscura females approached males more often than did D. melanogaster females, and male D. hydei approached females as often as males of the other two species, both results inconsistent with parental investment theory. Male D. pseudoobscura and D. hydei were more likely to approach males in same-sex pairs than male D. melanogaster , inconsistent with parental investment theory.     

Lifetime success and interactions of farm salmon invading a native population

Farm Atlantic salmon escape and invade rivers throughout the North Atlantic annually, which has generated growing concern about their impacts on native salmon populations. A large-scale experiment was therefore undertaken in order to quantify the lifetime success and interactions of farm salmon invading a Norwegian river. Sexually mature farm and native salmon were genetically screened, radio tagged and released into the River Imsa where no other salmon had been allowed to ascend. The farm fishes were competitively and reproductively inferior, achieving less than one-third the breeding success of the native fishes. Moreover, this inferiority was sex biased, being more pronounced in farm males than females, resulting in the principal route of gene flow involving native males mating with farm females. There were also indications of selection against farm genotypes during early survival but not thereafter. However, evidence of resource competition and competitive displacement existed as the productivity of the native population was depressed by more than 30%. Ultimately, the lifetime reproductive success (adult to adult) of the farm fishes was 16% that of the native salmon. Our results indicate that such annual invasions have the potential for impacting on population productivity, disrupting local adaptations and reducing the genetic diversity of wild salmon populations.     

Sexual Selection in Black Morph Girardinus metallicus (Pisces: Poeciliidae): Females Can Spot a Winner (But We Cannot)

Male–male competition may interfere with the ability of females to choose mates by interrupting courtship or by favoring highly aggressive males who may damage females during mating attempts. Alternatively, females may benefit by mating with dominant males, and female choice and male–male competition may therefore act in unison. The same traits, including aggressiveness, may indicate male quality to females and to rivals. We investigated sexual selection in the black morph of the endemic Cuban poeciliid fish, Girardinus metallicus, to ascertain the links between morphological and behavioral traits and success in intra‐ and intersexual selection. Males conspicuously exhibit their black ventral surface and gonopodium to females during courtship. Dichotomous choice tests revealed female association preferences for certain males, and those same males were more successful in monopolizing access to females when the fish were allowed to directly interact. Dominant males followed, courted, and copulated with females more than subordinate males within a pair, and it appears that females could either assess dominance based on cues we did not measure, or could influence subsequent mating success by their behavior during the dichotomous choice trials. There was an interaction between black status (i.e., whether the male in each pair had more or less ventral black coloration than the other male in that pair) and dominance, such that low‐black dominant males courted early and then shifted to following females, whereas high‐black dominant males courted far more later in the observation period. These results hint at the importance for sexual selection of the interplay between a static morphological trait (black coloration) and a dynamic behavioral trait (aggressiveness), but the functional significance of the courtship display remains a mystery.     

Mobility and Navigation among the Yucatec Maya

Sex differences in range size and navigation are widely reported, with males traveling farther than females, being less spatially anxious, and in many studies navigating more effectively. One explanation holds that these differences are the result of sexual selection, with larger ranges conferring mating benefits on males, while another explanation focuses on greater parenting costs that large ranges impose on reproductive-aged females. We evaluated these arguments with data from a community of highly monogamous Maya farmers. Maya men and women do not differ in distance traveled over the region during the mate-seeking years, suggesting that mating competition does not affect range size in this monogamous population. However, men’s regional and daily travel increases after marriage, apparently in pursuit of resources that benefit families, whereas women reduce their daily travel after marriage. This suggests that parental effort is more important than mating effort in this population. Despite the relatively modest overall sex difference in mobility, Maya men were less spatially anxious than women, thought themselves to be better navigators, and pointed more accurately to distant locations. A structural equation model showed that the sex by marital status interaction had a direct effect on mobility, with a weaker indirect effect of sex on mobility mediated by navigational ability.     

Resources,attractiveness, family commitment; reproductive decisions in human mate choice

This study of reproductive decisions in human mate selection used data from "lonely hearts" advertisements to examine a series of predictions based on the mate preferences of male and females relating to age; physical appearance; financial condition and socioeconomic status; family commitment and personal traits; short- and long-term mating; and marital status and preexisting children. The sample consisted of 1000 personal advertisements (500 male) placed in two daily, national papers between February and October 1994 in Hungary. The research procedure included a pilot study of 150 advertisers (75 male) to refine the categories examined. Analysis was performed using 1) a matrix with one axis referring to offers and the other to demands of males and females separately; 2) a matrix of offers only to derive correlated traits of claims by males and females; and 3) a matrix with columns describing sex, offers, demands, advertiser's age, and required age and a row for each of the 1000 samples. It was found that men preferred younger mates, while women preferred older ones. Men were more likely to seek physical attractiveness, while women were more likely to seek financial resources (ranked 7th) and high status (ranked 6th). Women strongly preferred male domestic virtue and family commitment, and twice as many women as men demanded long-term relationships. Women more frequently declared preexisting children, and men exhibited a reluctance to accept these children. Both males and females employed "trade-off" strategies, making greater demands if they felt they had attractive offers.     

Female rose bitterling prefer MHC-dissimilar males: experimental evidence

The role of genetic benefits in female mate choice remains a controversial aspect of sexual selection theory. In contrast to "good allele" models of sexual selection, "compatible allele" models of mate choice predict that females prefer mates with alleles complementary to their own rather than conferring additive effects. While correlative results suggest complementary genetic effects to be plausible, direct experimental evidence is scarce. A previous study on the Chinese rose bitterling (Rhodeus ocellatus) demonstrated a positive correlation between female mate choice, offspring growth and survival, and the functional dissimilarity between the Major Histocompatibility Complex (MHC) alleles of males and females. Here we directly tested whether females used cues associated with MHC genes to select genetically compatible males in an experimental framework. By sequentially pairing females with MHC similar and dissimilar males, based on a priori known MHC profiles, we showed that females discriminated between similar and dissimilar males and deposited significantly more eggs with MHC dissimilar males. Notably, the degree of dissimilarity was an important factor for female decision to mate, possibly indicating a potential threshold value of dissimilarity for decision making, or of an indirect effect of the MHC.     

Male aggressive behavior and exaggerated hindlegs of the bean bug Riptortus pedestris

Males of the bean bug species Riptortus pedestris possess larger hindlegs than females. Observations of male-male interactions showed that the enlarged hindlegs are used as weapons in male fights, and that males with larger hindlegs win fights more frequently. Morphological analysis based on the positive allometry test showed that the femora of larger males are relatively bigger than those of smaller males, but femora of larger females are not relatively larger than those of smaller females. These results suggest that sexual selection in R. pedestris favors larger hindlegs for male fighting. In addition, the thorax and abdomen lengths were larger in the male than in the female. The males often lift their abdomen with their back to the opponent for displays against an opponent. As a result, abdominal size may be under stronger selection in the male than in the female, as for the exaggerated hindlegs.     

Sexual differences in gas exchange and response to environmental stress in dioecious Silene latifolia (Caryophyllaceae)

Females of dioecious species usually have higher reproductive effort than males because they produce fruits in addition to flowers. Since females have higher reproductive effort, they are expected to be more negatively affected than males by low resource availability. We tested that assumption by growing females and males of Silene latifolia under low levels of light, water, nitrogen, phosphorus, and potassium. Gas exchange of the sexes did not respond differently to low resource availability; higher female reproductive effort relative to males did not differentially affect their ability to assimilate carbon. However, male photosynthesis rates and stomatal conductances were slightly, but consistently, higher than those of females. The intersexual difference in photosynthesis rate may be a proximate result of reproduction if females translocate nutrients, particularly nitrogen, from their leaves to developing fruits. Alternatively (or perhaps additionally), higher male photosynthesis and stomatal conductances relative to females may be the ultimate result of sexual selection. This could be the case if 1) reproductive effort as estimated by biomass allocation is misleading and males actually invest more in reproduction than females, or 2) females experience stronger selection than males to conserve water late in the growing season, when soil moisture is likely to be low but females need to complete fruit maturation. Our results indicated that females had slightly lower leaf nitrogen but higher photosynthetic water-use efficiency than males, so it is possible that both proximate and ultimate factors are operating simultaneously to cause lower female photosynthesis rates.     

Tail Length and Mutual Mate Choice in Bearded Tits (Panurus biarmicus)

Direct sexual selection via mutual mate choice can result in both sexes showing conspicuous traits. We experimentally tested whether this hypothesis can explain tail length in the bearded tit (Panurus biarmicus). In this species, both sexes have a long, graduated tail. Males have, however, a longer tail than females, suggesting perhaps that females are choosier than males in selecting mates. We used two choice set‐ups for each sex: shortened vs. control tail individuals and elongated vs. control tail individuals. We found that direct sexual selection seems to operate differently in the two sexes. In both set‐ups, females spent more time with the male with the longest tail, and they also showed sexual display behaviour only towards these males. Males spent more time with control than with short‐tailed females, but they did not discriminate between control and long‐tailed females. Moreover, males displayed preference towards both short‐ and long‐tailed females. Thus, females preferred long‐tailed males, whereas males did not always prefer long‐tailed females. Our study suggests that mutual mate choice has played a role in the evolution of long tails in bearded tits. It also suggests that the sexual dimorphism in tail length has evolved because mate choice exerts a stronger sexual selection pressure on males than on females.     

Sexual size dimorphism and sexual selection in turtles (order testudines)

Summary This paper combines published and original data on sexual size dimorphism, reproductive behavior, and habitat types in turtles. Our major finding is that observed patterns of sexual size dimorphism correlate with habitat type and male mating strategy. (1) In most terrestrial species, males engage in combat with each other. Males typically grow larger than females. (2) In semiaquatic and bottom-walking aquatic species, male combat is less common, but males often forcibly inseminate females. As in terrestrial species, males are usually larger than females. (3) In truly aquatic species, male combat and forcible insemination are rare. Instead, males utilize elaborate precoital displays, and female choice is highly important. Males are usually smaller than females.We interpret these correlations between sexual behavior and size dimorphism in terms of sexual selection theory: males are larger than females when large male size evolves as an adaptation to increase success in male combat, or to enable forcible insemination of females. In contrast, males are usually smaller than females where small size in males evolves to increase mobility (and hence, ability to locate females), or because selection for increased fecundity may result in increased female size. In turtle species with male combat or forcible insemination, the degree of male size superiority increases with mean species body size.     

No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.     

Sexual Selection and Breeding Patterns: Insights from Salmonids (Salmonidae)

Although "intrasexual selection" has been accepted as the mechanism by which males evolve elaborate secondary sexual traits which are used in aggressive contests, the importance of "intersexual selection" as a mechanism by which males have acquired exaggerated traits to display to females during courtship was less readily accepted. In spite of this scepticism, several genetic models have supported the latter idea, and many empirical studies showed that females were generally more discriminating in mate choice than males, because of differences in relative investment between sexes. Nowadays, this idea is reinforced by various concepts (parental investment, potential reproductive rate, environmental potential for polygamy...) which stress that the strength of sexual selection is related to many interdependent factors, such as mating systems, resource distribution (food, habitat, mate), life history and other ecological characteristics. The case of Salmonids is presented here to show how novel information on sexual selection has contributed to the understanding of the plasticity of breeding patterns in the context of evolutionary biology.     

The Role of Courtship Behavior and Size in Mate Preference in the Sex‐Role‐Reversed Gulf Pipefish,Syngnathus scovelli

In sex‐role‐reversed species, sexual selection acts more strongly on females than on males, a situation that can result in the evolution of secondary sexual traits in females and strong mating preferences in males. While some research exploring mating preferences in sex‐role‐reversed species has been conducted, overall, this topic remains relatively unexplored. The Gulf pipefish, Syngnathus scovelli, is a highly polyandrous pipefish species. Sexual selection is significantly stronger in females than in males, which has led to the evolution of both morphological and behavioral female secondary sexual traits. However, because males gestate the offspring in specialized pouches and make a substantial investment in embryos during development, females may also benefit from being choosy. The goal of this study was to examine both male and female mating preferences in this species. We found that male mating preference was significantly associated with female courtship behavior. Larger females were also able to maintain these behaviors for longer intervals than smaller females. No evidence of female mating preference in regard to male size was observed but the data suggest that male behaviors may be providing positive reinforcement to courting females. This research provides further insight into how mate preferences vary among sex‐role‐reversed species.     

Causes of a non-random pairing by size in the brine shrimp,Artemia salina: (Crustacea: Anostraca)

Summary Brine shrimp (Artemia salina) males and females entered precopula assortatively by size in the laboratory; large males also had a pairing advantage over smaller males. We investigated the causes of such nonrandom pairing to test hypotheses on size-assortative mating.We found precopulatory biases with respect to male size in the absence of direct competition among males (which produces pairing biases in other species). Large males encountered females significantly more often than did small males. Similarly, large females encountered males more often than did small females, but showed less willingness than small females to enter precopula when housed with small males. Consequently, large females took longer than small females to enter precopula with small males. Although large males entered precopula readily with small females, such size-mismatched pairs appeared short-lived.We conclude that non-random pairing by size in A. salina is determined by several factors including: encounter rates between males and females of different sizes, female behavior, and time following initial pair formation. Our results are likely applicable to other species and can help explain variation for selection on size or other traits.     

The evolution of sexual dimorphism in parasitic cuckoos: sexual selection or coevolution?

Sexual dimorphism is ubiquitous in animals and can result from selection pressure on one or both sexes. Sexual selection has become the predominant explanation for the evolution of sexual dimorphism, with strong selection on size-related mating success in males being the most common situation. The cuckoos (family Cuculidae) provide an exceptional case in which both sexes of many species are freed from the burden of parental care but where coevolution between parasitic cuckoos and their hosts also results in intense selection. Here, we show that size and plumage differences between the sexes in parasitic cuckoos are more likely the result of coevolution than sexual selection. While both sexes changed in size as brood parasitism evolved, we find no evidence for selection on males to become larger. Rather, our analysis indicates stronger selection on parasitic females to become smaller, resulting in a shift from dimorphism with larger females in cuckoos with parental care to dimorphism with larger males in parasitic species. In addition, the evolution of brood parasitism was associated with more cryptic plumage in both sexes, but especially in females, a result that contrasts with the strong plumage dimorphism seen in some other parasitic birds. Examination of the three independent origins of brood parasitism suggests that different parasitic cuckoo lineages followed divergent evolutionary pathways to successful brood parasitism. These results argue for the powerful role of parasite-host coevolution in shaping cuckoo life histories in general and sexual dimorphism in particular.     

Sex and Weapons: Contrasting Sexual Dimorphisms in Weaponry and Aggression in Snapping Shrimp

Sexual dimorphisms in weaponry and aggression are common in species in which one sex (usually males) competes for access to mates or resources necessary for reproduction – sexually dimorphic weaponry and aggression, in other words, are frequently the result of intrasexual selection. In snapping shrimp, the major chela (snapping claw) can be a deadly weapon, and males of many species have larger chelae than females, a pattern readily interpreted as resulting from intrasexual selection. Thus, males might be expected to show more sex‐specific aggression than females, and be more aggressive overall. We tested these predictions in two species of snapping shrimp in a territorial defense context. Neither of these predictions was supported: in both species, females, but not males, engaged in sex‐specific aggression and females were more aggressive than males overall. These contrasting sexual dimorphisms – larger weaponry in males but higher aggression in females – highlight the importance of considering the function of weaponry and aggression in contexts other than direct competitions over mates. In addition, species differences in the degree of sexual dimorphism in chela size were due to differences in female, not male, chela size, and the species with greater sexual dimorphism in weaponry was significantly less aggressive overall; also, while paired and solitary males did not differ in residual chela size, for the species with greater sexual dimorphism, females carrying embryos had smaller residual chela sizes. These results suggest that understanding the sexual dimorphisms in weaponry and aggression in snapping shrimp requires understanding the relative costs and benefits of both in females as well as males.     

Sexual selection on cuticular hydrocarbons of male sagebrush crickets in the wild

Cuticular hydrocarbons (CHCs) play an essential role in mate recognition in insects but the form and intensity of sexual selection on CHCs has only been evaluated in a handful of studies, and never in a natural population. We quantified sexual selection operating on CHCs in a wild population of sagebrush crickets, a species in which nuptial feeding by females imposes an unambiguous phenotypic marker on males. Multivariate selection analysis revealed a saddle-shaped fitness surface, suggesting a complex interplay between the total abundance of CHCs and specific CHC combinations in their influence on female choice. The fitness surface resulting from two axes of disruptive selection reflected a trade-off between short- and long-chained CHCs, suggesting that males may be sacrificing some level of desiccation resistance in favour of increased attractiveness. There was a significant correlation between male body size and total CHC abundance, suggesting that male CHCs provide females with a reliable cue for maximizing benefits obtained from males. Notwithstanding the conspicuousness of males’ acoustic signals, our results suggest that selection imposed on males via female mating preferences may be far more complex than previously appreciated and operating in multiple sensory modalities.     

Sexually dimorphic mate preference in Japan

Lonely hearts advertisements (LHA) published in Japan were examined in a comparative study on sexually dimorphic mate preference. I analyzed 944 LHA written by Japanese (730 by males and 214 by females) seeking short-term relationships and 780 LHA (577 by males and 203 by females) seeking long-term relationships. Some universal patterns of mate preference were confirmed and others were not. Female advertisers in both categories sought more traits than they offered; they also sought more traits than male advertisers. Males tended to offer their financial and social status, and females tended to seek those traits. More females requested family commitment than males. While there was no sex difference in offering and seeking physical appearance and health, females tended to request photographs of their potential mates. Males were more likely than females to be willing to accept children from previous relationships, although there was no significant difference in refusing such children. More females seeking long-term mates requested family commitment than females seeking short-term mates. In both males and females, more advertisers seeking long-term mates offered family commitment than advertisers seeking short-term mates. Some predictions for contingent preference were also examined. One prediction confirmed was that females offering physical appearance and health sought more traits than those not doing so. However, males offering financial and social status did not make higher demands than those who did not, which does not support one prediction. This paper was presented in a meeting of a team research project on "Mating systems, mate choice, and evolution by sexual selection in humans" by the International Research Center for Japanese Studies. I appreciate Professor Takeru Akazawa and other members inviting me to the project. Ryo Oda obtained his Ph.D. from the University of Tokyo for the study of lemur vocal communication. He is a lecturer at Nagoya Institute of Technology, and his current work focuses on the evolution of human behavior and language.     

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.