Giant males or dwarf females: what determines the extreme sexual size dimorphism in Lamprologus callipterus?

In the Lake Tanganyika cichlid Lamprologus callipterus , males were >12 times heavier than females, the most extreme sexual size dimorphism in this direction among animals. L. callipterus males construct nests of empty snail shells in which the females breed. If the ancestors of L. callipterus were small cichlids, both sexes may have used shells for shelter. If the ancestors were larger, snail shells could not be used as shelters and would be important only for reproduction. In the field and the laboratory, females bred only in shells and the largest spawned in the largest shells. In the field, females chose larger shells than the average available in males' territories and did not copy the mate choice of other females. They never hid from predators in snail shells and they occurred commonly in areas without any potential shell shelters. In laboratory experiments females used shells only for reproduction and hardly for shelter. Therefore, it seems unlikely that L. callipterus descended from small shell-brooding cichlids which used shells for shelter, but more likely that the ancestors were of large or intermediate size, and that female size is constrained by the sizes of snail shells, which appear to be optimal breeding substrata.     

Sexual conflict over breeding substrate causes female expulsion and offspring loss in a cichlid fish

Females of the Lake Tanganyika cichlid Lamprologus callipterusexclusively breed in empty snail shells that males collect intheir territories. Male–male competition for shells issevere, leading to frequent shell stealing and territory takeover.As a consequence, males have breeding females in their shellsthat spawned with competitors. In this field study, we investigatedboth naturally occurring and experimentally induced encountersof territorial males with females that had spawned with othermales. We found that the breeding success of females that weretaken over by a different male was significantly reduced. Behavioralobservations after experimental shell relocation further showedthat males recognized females that they had not spawned with:males directed more exploration and manipulation behavior towardsuch shells compared with controls. Reoccupation rate of emptiedexperimental shells was significantly higher than that of unmanipulatedempty shells. This indicates that shell stealing and nest takeover,followed by female expulsion, contribute to the reproductivesuccess of L. callipterus males. We also found that female matechoice reduces expulsion risk: females preferred to mate withlarge males, and male size correlated with dominance. We concludethat the limited availability of breeding substrate is a keydeterminant of both intrasexual competition and intersexualconflict in this species.     

Some evidence for different ecological pressures that constrain male and female body size

The dwarf morph of the Lake Tanganyika cichlid Telmatochromis temporalis uses empty snail shells as shelters and breeding sites in shell beds, in which many empty shells exist. Here, we assessed selection forces regulating body size in this fish. Field observations showed that large males tended to have a greater number of females in their territories, suggesting that sexual selection favours large males. Nonetheless, a transplant experiment suggested that male body size was limited by the ability to hide in empty shells from large piscivorous fish. In females, the number of ovarian eggs increased with body size, suggesting that fecundity selection favours large females. However, females are smaller than males. Females spawned eggs close to the apices inside the shells. The small space there would decrease the risk of egg predation by egg predators, and small body size of females may be a result of adaptation to spawn eggs in the small, safe spaces. This study provides support for the idea that male and female body sizes have been limited by different ecological pressures (predation on adult fish in males, predation on eggs in females), which has not been reported previously in any animal.     

Seasonal dimorphism in the horny bills of sparrows

Bill size is often viewed as a species‐specific adaptation for feeding, but it sometimes varies between sexes, suggesting that sexual selection or intersexual competition may also be important. Hypotheses to explain sexual dimorphism in avian bill size include divergence in feeding niche or thermoregulatory demands, intrasexual selection based on increased competition among males, or female preference. Birds also show seasonal changes in bill size due to shifts in the balance between growth rate and wear, which may be due to diet or endogenous rhythms in growth. Insight into the function of dimorphism can be gained using the novel approach of digital x‐ray imaging of museum skins to examine the degree to which the skeletal core or the rhamphotheca contribute to overall dimorphism. The rhamphotheca is ever‐growing and ever‐wearing, varying in size throughout life; whereas the skeletal core shows determinant growth. Because tidal marsh sparrows are more dimorphic in bill size than related taxa, we selected two marsh taxa to investigate dimorphism and seasonality in the size of the overall bill, the skeletal core, and the rhamphotheca. Bill size varied by sex and season, with males having larger bills than females, and bill size increasing from nonbreeding to breeding season more in males. Skeletal bill size varied with season, but not sex. The rhamphotheca varied primarily with sex; males had a larger rhamphotheca (corrected for skeletal bill size), which showed a greater seasonal increase than females. The rhamphotheca, rather than the skeletal bill, was responsible for sexual dimorphism in overall bill size, which was particularly well developed in the breeding season. The size of the rhamphotheca may be a condition‐based character that is shaped by sexual selection. These results are consistent with the evidence that bill size is influenced by sexual selection as well as trophic ecology.     

The adaptive significance of electrophoretic mobility in phosphoglucose isomerase (PGI)

Sexual dimorphism in size and plumage was investigated in the lek-breeding Jackson's widowbird Euplectes jacksoni. Size dimorphism was evident from the sexual difference in tarsus length, reflecting skeletal body size. The long tail and the wide collar of breeding plumaged males were obvious secondary sex traits, but the wing was also longer than in subadults and might likewise be sexually selected (i.e. not merely a byproduct of body size). Possibly, the increased wingspan functions to save energy during the jump display. To reveal intrasexual selection, courtholders were compared with floaters (nuptial males captured off the leks), and were found to be larger in body size, wing length, collar and tail. The roles of inter-and intrasexual selection are discussed with reference to previously demonstrated female choice, and new results indicating competition for access to leks: quick reoccupation of deserted display courts, frequent observations of intruders and a finding that central males were more aggressive than peripherals. Observations imply that the collar is an agonistic signal that is neutral with respect to female choice. Possible contributions of natural selection to the sexual dimorphism are also considered.     

Body size evolution of a shell‐brooding cichlid fish from Lake Tanganyika

The substrate‐brooding cichlid fish Telmatochromis temporalis in Lake Tanganyika demonstrates a simple example of ecological speciation between normal and dwarf morphs through divergent natural selection on body size. The dwarf morph most likely evolved from the ancestral normal morph; therefore, elucidating the evolution of its small body size is a key to understanding this ecological speciation event. Previous studies suggest that the small body size of the dwarf morph is an adaptation to the use of empty snail shells as shelters (males) and spawning sites (females), but this idea has not been fully evaluated. Combining original and previously published information, this study compared likelihood values to determine the primary factor that would be responsible for regulating the body size of the dwarf morph. Male body size is most likely regulated by the ability to turn within shells, which may influence the predation avoidance of adult fish. Females are smaller than males, and their body size is most likely regulated by the ability to lay eggs in the small spaces within shells close to the shell apices where predation risk on eggs is lower. This study provides new evidence supporting the hypothesis that different natural selection factors affected body size of the different sexes of the dwarf morph, which has not been reported in other animal species.     

Paternal inheritance of growth in fish pursuing alternative reproductive tactics

In species with indeterminate growth, age‐related size variation of reproductive competitors within each sex is often high. This selects for divergence in reproductive tactics of same‐sex competitors, particularly in males. Where alternative tactics are fixed for life, the causality of tactic choice is often unclear. In the African cichlid Lamprologus callipterus, large nest males collect and present empty snail shells to females that use these shells for egg deposition and brood care. Small dwarf males attempt to fertilize eggs by entering shells in which females are spawning. The bourgeois nest males exceed parasitic dwarf males in size by nearly two orders of magnitude, which is likely to result from greatly diverging growth patterns. Here, we ask whether growth patterns are heritable in this species, or whether and to which extent they are determined by environmental factors. Standardized breeding experiments using unrelated offspring and maternal half‐sibs revealed highly divergent growth patterns of male young sired by nest or dwarf males, whereas the growth of female offspring of both male types did not differ. As expected, food had a significant modifying effect on growth, but neither the quantity of breeding substrate in the environment nor ambient temperature affected growth. None of the environmental factors tested influenced the choice of male life histories. We conclude that in L. callipterus growth rates of bourgeois and parasitic males are paternally inherited, and that male and female growth is phenotypically plastic to only a small degree.     

Body size variation in the sexually dimorphic scaphopod Rhabdus rectius (Carpenter, 1864) (Dentaliida: Rhabdidae)

ABSTRACT

Male-biased sexual size dimorphism typically evolves via sexual selection for larger males that are favoured by choosy females or are more successful in mate competition with other males. Among marine invertebrates that broadcast their gametes into the ocean for fertilisation, this form of sexual size dimorphism is rare because such species lack direct interactions among males or between the sexes. However, the broadcast-spawning tusk shell Rhabdus rectius was recently reported to show strong male-biased sexual size dimorphism. That pattern might imply interesting and undiscovered sexual selection in this species. We found instead that the distribution of body size variation (weight, shell length) was similar between males and females of R. rectius, and mean sizes were not different between the sexes. However, we noted a male-biased sex ratio (～1:1.3) in our large sample of individuals. Many live scaphopods (and several dead shells) showed partial or complete boreholes drilled by predatory gastropods. Boreholes were observed on males and females in similar proportions. We collected scaphopods along with multiple individuals of one likely scaphopod predator, the small moon snail Euspira pallida, and in the lab we observed successful attacks by moon snails on tusk shells.     

Genetic and social control of male maturation in Phallichthys quadripunctatus (Pisces: Poeciliidae)

Age and size at maturity can have significant fitness consequences. Selection often favors early-maturing individuals because of their higher survival to maturity and greater relative contribution to population growth rate, but it may also favor delayed maturation if fitness increases with age or size at maturity. Males of several poeciliid fishes exhibit variation in age and size at maturity primarily controlled by a sex-linked gene called the P-locus. Wild-caught Phallichthys quadripunctatus males show a bimodal size distribution, which is often associated with a P-locus polymorphism in other poeciliids. We conducted two experiments to evaluate the inheritance of male age and size at maturity and the influence of social environment (presence of mature or juvenile males during development) on these traits. We specifically tested the hypothesis that male age and size at maturity in P. quadripunctatus are governed by a single Y-linked locus, and modified by the social environment. Although our results imply both a genetic and an environmental component to the dimorphism in maturation, both large and small males were able to sire both large and small sons, allowing us to reject the hypothesis that age and size at maturity in this species are controlled by a single, Y-linked locus. Our data do not conform adequately to any of the genetic mechanisms described to date for maturation polymorphism in poeciliids. We suggest alternative mechanisms that may operate in P. quadripunctatus.     

Quantitative genetics of costly neonatal sexual size dimorphism in squirrel monkeys (Saimiri boliviensis)

Offspring size is often an intimate link between the fitness of parents and offspring. Among mammals, neonate mass is also related to adult levels of dimorphism and intrasexual competitive mating. We describe the sex‐specific genetic architecture of neonate mass in captive squirrel monkeys (Saimiri boliviensis), a small Neotropical primate. Best fitting quantitative genetic models show strong maternal genetic effects with little difference between sexes offering limited opportunity for neonatal dimorphism to respond to observed or hypothetical selection. Heritabilities that are approximately zero also imply it is unlikely that neonatal dimorphism can evolve as a correlated response to selection on adult size. However, male mass is also more dependent on maternal condition (age and parity) making dimorphism plastic. Finally, we hypothesize that large maternal genetic effects reflect income breeding and tightly synchronized seasonal reproduction in squirrel monkeys, both of which require strong maternal control of offspring growth and timing of birth.     

Size-Related Advantages for Reproduction in a Slightly Dimorphic Raptor: Opposite Trends between the Sexes

Despite many comparative analyses and more than 20 proposed hypotheses, there is still little consensus over the factors promoting the evolution of reversed sexual dimorphism (RSD) in raptorial species. Furthermore, intrapopulation studies, which may elucidate how RSD is maintained once evolved, have been surprisingly scarce and only focused on a handful of species with medium to high dimorphism. We examined the reproductive advantages associated with body size and condition, measured in the pre‐laying period, in a diurnal raptor with low sexual dimorphism, the black kite (Milvus migrans). The study population was essentially monomorphic in size. For females, there was an evidence of reproductive benefits associated with larger size and/or with better body condition. Larger females had also access to higher quality partners and territories, consistent with the ‘intrasexual selection’ hypothesis, by which members of the larger sex enjoy size‐related advantages in intrasexual competition over a scarce resource, the smaller sex. Opposite trends emerged for males: smaller, leaner males had higher breeding output, consistent with the ‘small efficient male’ hypothesis. Overall, the fact that we observed in an essentially monomorphic population the same selection pressures previously found in species with marked dimorphism suggests that such reproductive advantages may be counterbalanced in our study model by opposite selection pressures during other stages of the life cycle. This casts some doubts on the evolutionary significance of studies focusing exclusively on reproduction and calls for the need of more comprehensive analyses incorporating trait‐mediated differentials in survival and recruitment.     

Genetic constraints on floral evolution in a sexually dimorphic plant revealed by artificial selection

Sexual dimorphism is one of the most widespread and recognizable patterns of phenotypic variation in the biotic world. Sexual dimorphism in floral display is striking in the dioecious plant Silene latifolia, with males making many, small flowers compared to females. We investigated this dimorphism via artificial selection on two populations to determine whether genetic variation exists within populations for flower size and the extent of the between-sex correlation, whether a flower size and number trade-off exists within each sex, and whether pollen and ovule production vary with flower size. We selected for decreased flower size (calyx width) in females and increased flower size in males and measured the response to selection in size and correlated responses in flower dry mass, flower number, and pollen or ovule number per flower. Four bouts of selection in each of two selection programs were performed, for a total of three selection lines to decrease size, three to increase it, and two control lines. Flower size always significantly responded to selection and we always found a significant correlated response in the sex not under selection. Selection decreased but did not eliminate the sexual dimorphism in flower dry mass and number. A negative relationship between flower size and number within each sex was revealed. Whereas ovule number showed a significant correlated response to selection on flower size, pollen number did not. Our results indicate that although substantial additive genetic variation for flower size exists, the high between-sex genetic correlation would likely constrain flower size from becoming more sexually dimorphic. Furthermore, floral display within each sex is constrained by a flower size and number trade-off. Given this trade-off and lack of variation in pollen production with flower size, we suggest that sexual dimorphism evolved via sexual selection to increase flower number in males but not females.     

Development of intraspecific size variation in black coucals,white-browed coucals and ruffs from hatching to fledging

Most studies on sexual size dimorphism address proximate and functional questions related to adults, but sexual size dimorphism usually develops during ontogeny and developmental trajectories of sexual size dimorphism are poorly understood. We studied three bird species with variation in adult sexual size dimorphism: black coucals (females 69% heavier than males), white-browed coucals (females 13% heavier than males) and ruffs (males 70% heavier than females). Using a flexible Bayesian generalized additive model framework (GAMM), we examined when and how sexual size dimorphism developed in body mass, tarsus length and bill length from hatching until fledging. In ruffs, we additionally examined the development of intrasexual size variation among three morphs (Independents, Satellites and Faeders), which creates another level of variation in adult size of males and females. We found that 27–100% of the adult inter- and intrasexual size variation developed until fledging although none of the species completed growth during the observational period. In general, the larger sex/morph grew more quickly and reached its maximal absolute growth rate later than the smaller sex/morph. However, when the daily increase in body mass was modelled as a proportion, growth patterns were synchronized between and within sexes. Growth broadly followed sigmoidal asymptotic models, however only with the flexible GAMM approach, residual distributions were homogeneous over the entire observation periods. These results provide a platform for future studies to relate variation in growth to selective pressures and proximate mechanisms in these three species, and they highlight the advantage of using a flexible model approach for examining growth variation during ontogeny.     

Rapid evolutionary change in a sexual signal: genetic control of the mutation 'flatwing' that renders male field crickets (Teleogryllus oceanicus) mute

Colonizing events may expose organisms to physical and ecological environments found nowhere else in their range. Novel selection pressures can then influence subsequent rapid evolutionary changes. Here, I investigate the genetics of one such rapid change in the sexual signal of Polynesian field crickets, Teleogryllus oceanicus, that recently colonized the Hawaiian Islands. In Hawaii, T. oceanicus encounter a deadly parasitoid fly found nowhere else in their range. In <20 generations, a wing mutation, flatwing, that eliminates the crickets' song, an important sexual signal, but protects them from the fly, spread to >90% of males on the island of Kauai. I show, using crosses between flatwing males and females from a population that has never contained flatwings, that the song-suppressing mutation is due to a change in a single sex-linked locus. Contemporary evolution of secondary sexual characteristics has only rarely been identified as the result of single-gene changes and never before as a single sex-linked locus, but sex-linked inheritance is thought to facilitate the rapid evolution of these types of traits. Because divergence of sexual signals can influence reproductive isolation, understanding how colonization events and subsequent selection affect signals, and the genetic mechanisms of such change, can shed light on processes likely to play a role in speciation.     

Unusual allometry for sexual size dimorphism in a cichlid where males are extremely larger than females

When males are the larger sex, a positive allometric relationship between male and female sizes is often found across populations of a single species (i.e. Rensch’s rule). This pattern is typically explained by a sexual selection pressure on males. Here, we report that the allometric relationship was negative across populations of a shell-brooding cichlid fish Lamprologus callipterus, although males are extremely larger than females. Male L. callipterus collect and defend empty snail shells in each of which a female breeds. We found that, across six populations, male and female sizes are positively correlated with not only sexual and fecundity selection indices, but also with shell sizes. Given their different reproductive behaviours, these correlations mean that males are required to be more powerful, and thus larger, to transport larger shells, while female bodies are reduced to the shell size to enable them to enter the shells. Among the three size selections (sexual selection, fecundity selection and shell size), shell size explained the allometry, suggesting that females are more strongly subject to size selection associated with shell size availability than males. However, the allometry was violated when considering an additional population where size-selection regimes of males differed from that of other populations. Therefore, sexual size allometry will be violated by body size divergence induced by multiple selection regimes.     

Development and linkage mapping of novel sex-linked markers for marker-assisted cultivar breeding in pistachio (<Emphasis Type="Italic">Pistacia vera</Emphasis> L.)

The dioecious character of Pistacia vera L (the pistachio tree) limits its breeding capacity. Thus, early stage selection of males can save time, labor, and land. This study aimed to develop sex-linked single nucleotide polymorphism (SNP) markers, together with expressed sequence tag-derived simple sequence repeats (EST-SSRs), to determine position of the sex locus in pistachio by constructing a linkage map of its sex chromosome for the first time. Nine novel sex-linked SNP markers were successfully identified by SNaPshot minisequencing analysis of 25 SNP loci from 17 restriction site-associated DNA (RAD) reads in 309 individuals. All nine markers were heterozygous in females and homozygous in males supporting a ZW/ZZ sex determination system in pistachio. A total of 105 segregating SSRs and sex-linked markers were used to identify the sex chromosome and the position of the sex locus through analysis of a Siirt × Ba?yolu F₁ population with 122 progenies. Of these 105 markers, four common and four paternal SSRs were mapped onto the sex chromosome, along with the phenotypic sex locus and sex-linked markers. The resulting consensus map had a total length of 65.19 cM. The sex locus and sex-linked SNP markers were located in the center of the chromosome at a distance of 31.86 and 31.92 cM, respectively. This study presents valuable information about the sex chromosome and sex locus position as well as novel polymorphic EST-SSRs and nine sex-linked SNP markers in pistachio.     

Sexual Selection and Dynamics of Jaw Muscle in Tupinambis Lizards

Sexual dimorphism patterns provide an opportunity to increase our understanding of trait evolution. Because selective forces may vary throughout the reproductive period, measuring dimorphism seasonally may be an interesting approach. An increased male head size may be important in intersexual and intrasexual interactions. In Tupinambis lizards, a big head is attributed in part to a large adductor muscle mass. Competition for mating can differ in species with different sex ratio and different degrees of sexual size dimorphism. We examined sexual differences in mass of the pterygoideus muscle, its temporal variation throughout the reproductive period and the relationship between muscle and reproductive condition in Tupinambis merianae and T. rufescens. We characterized sexual size dimorphism and sex ratio in both species. Mature males had larger jaw muscles than mature females in both species, mainly during the reproductive season. The dimorphism in jaw muscle was due to an increase in muscle mass in sexually active males. Seasonal increases in muscle mass and variation between immature and mature individuals suggest that the jaw muscle might be a secondary sexual character. We propose that the pterygoideus muscle may act as a signal of reproductive condition of males because it is associated with testis size and sperm presence. The patterns of sexual dimorphism in jaw muscle in both species were similar; however, the comparison shows how sexual characters remain dimorphic in different competition contexts and in species with different degrees of body size dimorphism. Our results suggest that jaw muscle as sexual character could be influenced by inter- and intrasexual selective pressures.     

Selection on females can create 'larger males'

In many bird and mammal species, males are significantly larger than females. The prevailing explanation for larger-sized males is that sexual selection drives increased male size. In addition, researchers commonly assume that the extent of dimorphism indicates the strength of selection for increased size in males. Here, through reconstruction of ancestral morphology for males and females of one large avian clade we present data that contradict this assumption and illustrate that selection for decreased female size explains 'male-biased' dimorphism ca. 50% of the time. Our findings are also inconsistent with ecological niche partitioning between the sexes and increased breeding benefits from reduced female size as general explanations for the evolution of size dimorphism within the clade. We conclude that it is incorrect to assume sexual dimorphism results from a single selective factor, such as directional sexual selection on increased male size. Rather, we suggest that the selective forces leading to sexual dimorphism may vary between species and should be tested on a case-by-case basis using a phylogenetic approach.     

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.     

Size‐selective fishing affects sex ratios and the opportunity for sexual selection in Alaskan sockeye salmon Oncorhynchus nerka

Selective exploitation can cause adverse ecological and evolutionary changes in wild populations and also affect sex ratios but few studies have empirically documented skewed sex ratios in exploited fishes (other than species with extreme sexual size dimorphism, SSD). To investigate the possibility of sex‐selective fishing on Alaskan sockeye salmon Oncorhynchus nerka, we assessed sex ratios in fish at two spatial scales: within each of five fishing districts and among 13 breeding populations in one of these districts. We predicted that populations’ sex ratios would vary based on the average size of fish and SSD because size affects vulnerability to fishing. At the larger scale, we found a small but significant bias in fish returning to four of the five fishing districts (average = 52% females), and in four of the five districts males were caught at significantly higher rates than females. At the finer scale there was marked variation in sex ratio on the breeding grounds, ranging from 36% to 47% males. Populations with fish of intermediate sizes experienced the greatest sex ratio biases; the greater vulnerability of males than females to fishing resulted from a combination of larger SSD and different harvest rates between the sexes associated with the fishery size‐selectivity curve shape. Skewed sex ratios may change competition and behavior on the breeding grounds, relaxing selection on male traits associated with mate choice by females or intra‐sexual competition and altering demographic and evolutionary pressures on the fish. Assessment of the size selectivity of fishing gear and the population's SSD can help to illuminate if and how exploitation can affect sex ratios. Future studies examining size‐selective fishing should also evaluate the consequences for sex ratios, as this might help explain changes in harvested population structure and sustainability.