Male Morphological Traits Research Articles

Morphometric variation and deteriorating food availability both explain seasonally declining reproductive success of Dicrurus hottentottus (Hair-crested Drongo)

Abstract Seasonally declining reproductive performance in avian populations may be attributed to high-quality individuals breeding earlier than low-quality individuals (the quality hypothesis), to deteriorating environmental conditions (the date hypothesis), or both. By comparing the reproductive performance among different perennial pairs, and the same perennial pairs across different years, we tested the influence of timing of breeding on reproductive performance in Dicrurus hottentottus (Hair-crested Drongo) from 2010 to 2022. Breeding pairs that typically laid earlier relative to the population mean (i.e., early-breeding pairs) exhibited a significantly higher fledging rate compared to breeding pairs that often bred later relative to the population mean (i.e., late-breeding pairs). For a given pair, the fledging rate of early-breeding pairs increased when they bred later compared to other years, while the fledging rates of late-breeding pairs were significantly lower in years when they bred later than usual. We found that male morphological traits were associated with both the timing of breeding and the feeding rate. Pairs with long-billed (indicator of high quality) males bred earlier than pairs with short-billed males, and pairs with larger males (indicator of high quality) had a higher feeding rate than pairs with smaller males. Female age had reversed effects on the timing of breeding and fledging rate: older females tended to breed earlier than younger females; but there was a sharp decline in fledging rate after 7 years of age in late-breeding pairs. Finally, our results showed that the feeding rate and the amount of invertebrate biomass decreased with laying date, indicating deteriorating feeding conditions later in the breeding season. Overall, our findings support both the quality hypothesis and the date hypothesis. Low-quality D. hottentottus are likely to be most adversely affected by the phenological mismatches induced by climate change, which, in turn, may affect population dynamics through reduced fecundity.

Molecular differentiation analysis of ten putative species of Fannia (Diptera: Fanniidae) collected in carrion-baited traps from Colombia.

The genus Fannia is the most representative of the Fannidae family of true flies with worldwide distribution. Some species are attracted to decomposing materials and live vertebrate animals, which makes them important in forensics, medical and veterinary fields. However, identifying Fannia species can be difficult due to the high similarity in the external morphology of females and limited descriptions and morphological keys. Herein, molecular markers could provide a complementary tool for species identification. However, molecular identification has still limited application since databases contain few data for neotropical species of Fannia. This study assessed the potential of two molecular markers, the COI-3' region and internal transcribed spacer 2 (ITS2), to differentiate 10 putative species of the genus Fannia from Colombia using distance-based and tree-based approaches. The partial ITS2 and/or COI-3' regions allowed molecular diagnosis of six species, while pairs of species Fannia colazorrensis + F. dodgei and F. laclara + F. aburrae are conflicting. Although these results might suggest that conflicting pair species are conspecific, consistent morphological differences between males do not support this hypothesis. The lack of differentiation at the nuclear and mitochondrial molecular markers for the conflicting species may be due to incomplete evolutionary lineage separation, hybridization, or introgression events. In addition, sexual selection on male morphological traits before species-specific differences in molecular markers emerge may partially explain the results. Our study provides a valuable dataset to identify and confirm some Fannia species molecularly. Further, they could be used to associate females and immature stages with their conspecifics as a baseline to deep into their biology, ecology, distribution and potential applications in forensic and medico-veterinary entomology.

Female great tits (Parus major) reproduce earlier when paired with a male they prefer

AbstractMate choice is a key component of reproductive biology. Females often prefer certain males but do females modulate their reproductive investment depending on whether they are mated with their preferred partner? We investigated this question in great tits (Parus major) where we subjected 36 females to a six‐choice mate preference test. Male morphological traits and the female's own characteristics did not influence the preference females expressed. We however found that females spent more time near more exploratory males. We then paired females with one of the males in indoor aviaries, and subsequently monitored their reproductive investment (through measurement of plasma 17β‐oestradiol concentrations, first egg date, clutch size and egg size). Females that were mated with a male for which they had a strong preference laid their first clutch significantly earlier in the season than females paired with a male they less preferred. Our results show that mate preference influences reproductive investment in great tits, thereby linking mate choice to bird reproductive decisions.

Extra‐pair paternity is not repeatable between years in Pied Flycatchers (Ficedula hypoleuca): a role for social context

Extra‐pair paternity (EPP) is the consequence of the interactions between a social pair and extra‐pair males during the female's fertile phase in a specific social context and ecological environment. Although EPP occurs in many avian species, there is a lack of understanding of how environmental factors may impact its frequency. Accordingly, the relative importance of individual characteristics on the one hand, and of their immediate social environment on the other, may affect EPP repeatability and thereby the capacity of this trait to respond to selection. If EPP is an individual genetically based trait that may respond to selection, we expect it to be repeatable across breeding seasons. To check this possibility, we analysed the within‐individual repeatability in EPP of breeding males and females in two natural populations of Pied Flycatchers Ficedula hypoleuca in central Spain during three field seasons. We then studied the relationship between EPP and individual male and female traits (only some of which were themselves repeatable), as well as key context variables such as breeding synchrony and population density. Our results showed no repeatability for EPP in either sex. We found a positive association with laying date and stronger associations of EPP with male plumage and morphological traits than with female characteristics. We suggest that the variable social environment is an important modulator of EPP patterns, and that differences between field EPP studies in this respect may explain contradictory results in the same species, even in the same populations in different years.

From a pair to a dozen: the piscivorous species of Haplochromis (Cichlidae) from the Lake Edward system

Piscivory is a common trophic niche among cichlids of the East African Great Lakes, including Lakes Edward and George. From these two lakes, we examined the taxonomic diversity of cichlid species with a piscivorous morphology. Prior to this study, two piscivorous species were formally described, Haplochromis squamipinnis and H. mentatus. We redescribe both species and describe an additional ten new species of Haplochromis with a piscivorous morphology: H. latifrons sp. nov., H. rex sp. nov., H. simba sp. nov., H. glaucus sp. nov., H. aquila sp. nov., H. kimondo sp. nov., H. falcatus sp. nov., H. curvidens sp. nov., H. pardus sp. nov., and H. quasimodo sp. nov. All twelve species differ in dominant male colour pattern (unknown for H. latifrons sp. nov. and H. curvidens sp. nov.) and morphological traits. The species can be divided into two morphological groups: the macrodontic piscivores and the microdontic piscivores. This division potentially reflects an ecological differentiation in habitat use, hunting technique, prey species, and prey size. We conclude that some 12–20% of the species from the cichlid assemblage of Lake Edward have a piscivorous morphology.

Revealing diagnostic characters through morphological evolution in cleptoparasitic spider wasps (Hymenoptera, Pompilidae, Ceropales)

AbstractSpider wasps (Hymenoptera: Pompilidae) cleptoparasites, such as Ceropales Latreille, have evolved the ability to steal the spiders from other pompilids. This behaviour is often observed with morphological adaptations that might mislead taxonomic decisions due to convergence. For instance, four subgenera, Bifidoceropales Wolf, Ceropales s. str., Hemiceropales Wolf and Priesnerius Móczár and six species‐groups are recognized within Ceropales; all with doubtful identification. We studied species of Ceropales in light of molecular and morphological characters to delimit lineages and to test the applicability of morphological traits in diagnosing them. We used the molecular nuclear markers long‐wavelength rhodopsin and 28S ribosomal RNA, and the mitochondrial Cytochrome C Oxidase I available at Genebank to reconstruct Bayesian and maximum likelihood phylogenetic trees. Our results disagree with the current subgeneric classification. We found that fore wing venation and the shape of the female posterior metasomal segments are key characters to differentiate lineages. We discuss morphological evolution of the sting apparatus using ancestral state reconstructions; and we propose Bifidoceropales as a junior subjective synonym of Ceropales s. str., whereas Priesnerius, stat. resurr. and Hemiceropales are redefined based on male and female morphological traits. This study raises important concerns, from the validity of diagnostic characters currently used to identify cleptoparasite spider wasps—and taxa with habitat constraints leading to homoplasies. Taxonomy can benefit from the reconstruction of ancestral traits by revealing reliable diagnostic characters. Moreover, our investigation provides a framework for evolutionary studies on hymenopteran cleptoparasitoids and sets the basis for future phylogenomic investigations on Ceropales by opening new perspectives for taxonomic acts and guiding taxonomic sampling efforts.

Experimental immune challenges reduce the quality of male antennae and female pheromone output

Sexual signalling is a key feature of reproductive investment, yet the effects of immune system activation on investment into chemical signalling, and especially signal receiver traits such as antennae, are poorly understood. We explore how upregulation of juvenile immunity affects male antennal functional morphology and female pheromone attractiveness in the gumleaf skeletonizer moth, Uraba lugens. We injected final-instar larvae with a high or low dose of an immune elicitor or a control solution and measured male antennal morphological traits, gonad investment and female pheromone attractiveness. Immune activation affected male and female signalling investment: immune challenged males had a lower density of antennal sensilla, and the pheromone of immune-challenged females was less attractive to males than their unchallenged counterparts. Immune challenge affected female investment into ovary development but not in a linear, dose-dependent manner. While there was no effect of immune challenge on testes size, there was a trade-off between male pre- and post-copulatory investment: male antennal length was negatively correlated with testes size. Our study highlights the costs of elaborate antennae and pheromone production and demonstrates the capacity for honest signalling in species where the costs of pheromone production were presumed to be trivial.

Male morphology, performance and female mate choice of a swarming insect

Females of many species select mates based on important morphological and performance traits. This behaviour likely facilitates reproductive success thus exhibiting sexual selection. Most such studies have evaluated a single morphological variable, and only a minority of them studies the effects of behaviour and performance (functional capacity: Irschick et al., Evolutionary Ecology Research, 10, 177–196, 2008) at all. This study compares male morphological and performance traits differing in three variables that may correlate with fitness: condition index, flight ascent speed and resistance to torpor in relation to male mating success in the parasitoid wasp species Alabagrus texanus (Braconidae), a species where males swarm about emerging virgin females that display both choosy and non‐choosy behavioural phenotypes. Males that successfully mated with choosy females exhibited higher condition indices and somewhat stronger resistance to torpor than other males. Conversely, males that mated with non‐choosy females did not differ in any trait from other males we measured. Early‐arriving males did not have higher condition indices or greater mating success than other males. Thus, both morphological and performance traits contributed to male success, which acted through female choice, indicating a role for sexual selection. Patterns of choice further differed among females, independent of male traits.

Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate

Sexual selection favours traits that increase reproductive success via increased competitive ability, attractiveness, or both. Male rhesus macaque (Macaca mulatta) morphological traits are likely to reflect the effects of multiple sexual selection pressures. Here, we use a quantitative genetic approach to investigate the production and maintenance of variation in male rhesus macaque morphometric traits which may be subject to sexual selection. We collected measurements of body size, canine length, and fat, from 125 male and 21 female free-ranging rhesus macaques on Cayo Santiago. We also collected testis volumes from males. We used a genetic pedigree to calculate trait heritability, to investigate potential trait trade-offs, and to estimate selection gradients. We found that variation in most male morphometric traits was heritable, but found no evidence of trait trade-offs nor that traits predicted reproductive success. Our results suggest that male rhesus macaque morphometric traits are either not under selection, or are under mechanisms of sexual selection that we could not test (e.g. balancing selection). In species subject to complex interacting mechanisms of selection, measures of body size, weaponry, and testis volume may not increase reproductive success via easily-testable mechanisms such as linear directional selection.

Molecular phylogeny reveals the gradual evolutionary transition to soft-bodiedness in click-beetles and identifies sub-Saharan Africa as a cradle of diversity for Drilini (Coleoptera: Elateridae)

AbstractDrilini are soft-bodied predatory click-beetles (Elateridae: Agrypninae) with incompletely metamorphosed females. Due to divergent morphology, their classification has been contentious. We present the first densely sampled molecular phylogeny of Drilini based on nuclear and mitochondrial markers. Altogether, 44 species, representing all genera, were analysed using maximum likelihood and the Bayesian approach. Molecular analyses recovered five major clades that were also well supported by morphology. Afrotropical lineages mark deep splits. Most Palearctic species belong to a terminal clade. A few species of the predominantly Afrotropical Selasia are distributed from Arabia up to the Himalayas and Thailand. The origin of Drilini is dated to the Late Eocene (~35.5 Mya) and rapid radiation is identified from the Eocene/Oligocene to the Middle Miocene. We describe the gradual transformation of male morphological traits, e.g. the level of sclerotization, structure of mouthparts, loss of the thoracic interlocking mechanism, shortened elytra and expanded larviform abdomen. Five new genera, Austroselasia, Habeshaselasia, Illubaboria, Malacodrilus and Mashaselasia are proposed. Latoselasia, previously a subgenus of Wittmerselasia, is elevated to the genus rank. Five new species, Habeshaselasia nekemtensis, H. illubaborensis, Illubaboria bicolor, Malacodrilus hajeki and Mashaselasia aethiopica are described.

Song performance is a condition‐dependent dynamic trait honestly indicating the quality of paternal care in the bull‐headed shrike

The good parent hypothesis in sexual selection predicts that if females can increase their fitness by mating with males who provide high‐quality parental care, then female preferences for male phenotypes honestly indicating the quality of paternal care will evolve. In order to test this hypothesis, we investigated correlations between male song, the timing of pair formation of males, male feeding rate, and reproductive success, in the bull‐headed shrike Lanius bucephalus (an altricial oscine passerine with biparental care). Analysis revealed that although the timing of pair formation was not correlated with most song characteristics (e.g. repertoire size), male morphological traits (e.g. tail length), or male territory size, it was negatively correlated with male singing tempo (i.e. the number of notes uttered per second). Those males that sang at higher speeds were in better body condition (i.e. body mass standardized by tarsus length3 was higher), fed their chicks frequently during the nestling period, and raised heavy chicks. These results show that in the bull‐headed shrike male singing tempo is a condition‐dependent dynamic trait honestly indicating the quality of paternal care, and strongly supports the good parent hypothesis.

Social network predicts loss of fertilizations in nesting males of a fish with alternative reproductive tactics

Alternative reproductive tactics (ARTs) evolve when there is strong intra-sexual competition between conspecifics for access to mates. Typically, larger “bourgeois” males reproduce by securing the access to reproductive resources while smaller “parasitic” males reproduce by stealing fertilizations from larger males. A number of factors can influence the reproductive success of each tactic, including intrinsic (e.g. size) and extrinsic (e.g. tactic relative frequency) variables. An example where plastic ARTs occur is the peacock blenny Salaria pavo, with large males reproducing by defending nests and attracting females (bourgeois tactic) and small males reproducing by achieving sneaked fertilizations (parasitic tactic). In this study, we conducted field observations on individually tagged animals to determine their social network and collected eggs from 11 nests to determine the fertilization success of each male tactic. Paternity estimates for 550 offspring indicated an average fertilization success for nest-holder males of 95%. Nest-holder male morphological traits and social network parameters were tested as predictors of fertilization success, but only the number of sneakers present in the nest-holder’s social networks was found to be a predictor of paternity loss. Although male morphological traits had been previously found to be strongly correlated with reproductive success of nest-holder males, as measured by the number of eggs collected in the male’s nest, no correlation was found between any of the measured morphological traits and fertilization success for these males. The results suggest a stronger influence of the social environment than of morphological variables in the proportion of lost fertilizations by nest-holder males of this species.

Experimentally evolved and phenotypically plastic responses to enforced monogamy in a hermaphroditic flatworm.

Sexual selection is considered a potent evolutionary force in all sexually reproducing organisms, but direct tests in terms of experimental evolution of sexual traits are still lacking for simultaneously hermaphroditic animals. Here, we tested how evolution under enforced monogamy affected a suite of reproductive traits (including testis area, sex allocation, genital morphology, sperm morphology and mating behaviour) in the outcrossing hermaphroditic flatworm Macrostomum lignano, using an assay that also allowed the assessment of phenotypically plastic responses to group size. The experiment comprised 32 independent selection lines that evolved under either monogamy or polygamy for 20 generations. While we did not observe an evolutionary shift in sex allocation, we detected effects of the selection regime for two male morphological traits. Specifically, worms evolving under enforced monogamy had a distinct shape of the male copulatory organ and produced sperm with shorter appendages. Many traits that did not evolve under enforced monogamy showed phenotypic plasticity in response to group size. Notably, individuals that grew up in larger groups had a more male-biased sex allocation and produced slightly longer sperm than individuals raised in pairs. We conclude that, in this flatworm, enforced monogamy induced moderate evolutionary but substantial phenotypically plastic responses.

Simultaneous age-dependent and age-independent sexual selection in the lekking black grouse (Lyrurus tetrix).

Individuals' reproductive success is often strongly associated with their age, with typical patterns of early-life reproductive improvement and late-life senescence. These age-related patterns are due to the inherent trade-offs between life-history traits competing for a limited amount of resources available to the organisms. In males, such trade-offs are exacerbated by the resource requirements associated with the expression of costly sexual traits, leading to dynamic changes in trait expression throughout their life span. Due to the age dependency of male phenotypes, the relationship between the expression of male traits and mating success can also vary with male age. Hence, using longitudinal data in a lekking species with strong sexual selection - the black grouse Lyrurus tetrix - we quantified the effects of age, life span and age of first lek attendance (AFL) on male annual mating success (AMS) to separate the effects of within-individual improvement and senescence on AMS from selective (dis)appearance of certain phenotypes. Then, we used male AMS to quantify univariate and multivariate sexual selection gradients on male morphological and behavioural traits with and without accounting for age and age-related effects of other traits. Male AMS increased with age, and there was no significant reproductive senescence. Most males never copulated, and of the ones that did, the majority had only one successful year. Life span was unrelated to AMS, but early AFL tended to lead to higher AMS at ages 1-3. AMS was related to most morphological and behavioural traits when male age was ignored. Accounting for age and age-specific trait effects (i.e. the interaction between a trait and age) reduced the magnitude of the selection gradients and revealed that behavioural traits are under consistent sexual selection, while sexual selection on morphological traits is stronger in old males. Therefore, sexual selection in black grouse operates primarily on male behaviour and morphological traits may act as additional cues to supplement female choice. These results demonstrate the multifaceted influence of age on both fitness and sexual traits and highlight the importance of accounting for such effects when quantifying sexual selection.

Evolution of alternative male morphotypes in oxyurid nematodes: a case of convergence?

Male dimorphism has been reported across different taxa and is usually expressed as the coexistence of a larger morph with exaggerated male traits and a smaller one with reduced traits. The evolution and maintenance of male dimorphism are still poorly understood for several of the species in which it has been observed. Here, we analyse male dimorphism in several species of reptile parasitic nematodes of the genus Spauligodon, in which a major male morph (exaggerated morph), which presents the traditional male morphological traits reported for this taxon, coexists with a minor morph with reduced morphological traits (i.e. reduced genital papillae) resembling more closely the males of the sister genus Skrjabinodon than Spauligodon major males. Because of the level of uncertainty in the results of ancestral state reconstruction, it is unclear if the existence of male dimorphism in this group represents independent instances of convergent evolution or an ancestral trait lost multiple times. Also, although the number of major males per host was positively correlated with the number of females, the same did not hold true for minor males, whose presence was not associated with any other ecological factor. Nevertheless, the existence of male dimorphism in Spauligodon nematodes is tentatively interpreted as resulting from alternative reproductive tactics, with differences in presence and number of individuals as indicators of differences in fitness, with the lower numbers of minor males per host likely maintained by negative frequency-dependent selection.

Effects of Egg and Circulating Testosterone on Ring‐Necked Pheasant (Phasianus colchicus) Male Traits and Combat Outcome

AbstractStudies of avian species have shown that maternal effects mediated by the transfer of egg hormones can profoundly affect offspring phenotype and fitness. We previously demonstrated that the injection of a physiological amount of testosterone (T) in the eggs of ring‐necked pheasants (Phasianus colchicus) disrupted the covariation among male morphological traits at sexual maturity and positively affected male mating success. Here, we investigate whether egg T exposure affected adult male circulating T levels at the onset of the breeding season (reflecting gonadal maturation), and the relationship between circulating T and male traits. Egg T exposure did not affect pre‐mating plasma T. T levels were not associated with the expression of secondary sexual and non‐sexual traits or socio‐sexual behaviour (social rank, overall fighting ability and mating success). However, wattle brightness decreased with increasing circulating T in males hatched from T‐eggs (T‐males) but not among control males. In dyadic encounters during the peak mating period, control males with higher pre‐mating T levels had higher chances of being dominant over other control males. However, higher pre‐mating T levels did not predict success in male‐male competition in encounters involving T‐males. We suggest that the long‐term effects of egg T on male phenotype do not originate from differential gonadal maturation according to egg T treatment. Rather, prenatal androgens may have priming effects on functioning of target tissues, translating into differential phenotypic effects according to androgen exposure during embryonic development.

Dietary protein mediates a trade‐off between larval survival and the development of male secondary sexual traits

Summary Increased protein intake by adults typically enhances reproduction and shortens life, but much less is known about the effects of protein intake prior to reproductive maturity. In particular, it remains unclear whether dietary protein mediates a trade‐off between survival and the development of reproductive traits, especially in males. We used the nutritional geometry approach to investigate the effects of 25 replicated larval diets varying in protein and carbohydrate content on larval performance and the development of adult male morphology in the neriid fly Telostylinus angusticollis. We found that body size increased with carbohydrate and especially protein content in the larval diet. Moreover, after controlling for body size, dietary protein strongly enhanced the expression of those male morphological traits that appear to be most directly targeted by sexual selection, while having no effect on the expression of other traits. In sharp contrast, egg‐to‐adult viability decreased steeply with increasing protein content. Thus, protein intake during the larval stage mediates a trade‐off between the expression of male secondary sexual traits and the probability of survival to adult emergence.

Direct mate choice for simultaneous acoustic and visual courtship displays in the damselfish, Dascyllus albisella (Pomacentridae)

Acoustic signals are well established as key components of mate selection in terrestrial species, but not in aquatic species. It has long been known that damselfish (Pomacentridae) use a combined visual and acoustic display in their courtship.. This study examined several male qualities including individual size, courtship vigor, territory size and complexity, as well as components of the acoustic call including dominant frequency, pulse characteristics and repetition rate. The objective was to determine which male traits were correlated with mating success. Observations made over ten reproductive cycles revealed that female mate choices were not random and that male mating success was correlated with courtship rate (a simultaneous visual and acoustic cue) and the number of neighboring females, but not with male morphological traits, territory quality, or acoustic call structure. These results suggest that females choose mates based on a condition-dependent trait (courtship rate) that advertises quality of paternal care, which supports good parent models of sexual selection, thereby demonstrating the importance of the combined acoustic/visual display for sexual selection in fishes

Female mate choice based on territory quality in barn swallows

Female mate choice based on territory quality is difficult to study because territories often contain many resources, which are difficult to quantify. Here, using the barn swallow (Hirundo rustica gutturalis) breeding at an outdoor breeding site in Japan, where each male defends only a small territory containing old nests, we studied whether females choose social mates based on territory quality. Since the territories of this species contain few other resources, territory quality can easily be assessed by quantifying old nests in the territory. We made the following four observations: (1) male swallows displayed old nests in their territories to females; (2) the old nests used for the first clutch were less broken than the other old nests within the same territory; (3) territory quality, defined by the number of old nests weighted by the intactness of each old nest, predicted the productivity of the territory; and (4) males with better territories paired with females earlier, and hence bred earlier, than those with inferior territories. The relationships remained significant even after controlling for male morphological traits. Based on these results, we can infer that female swallows choose their mates based, in part, on territory quality.

Temporally Variable Multivariate Sexual Selection on Sexually Dimorphic Traits in a Wild Insect Population

A widely held view is that the strength and form of natural selection varies in time and space in response to varying ecological forces; however, adequate quantitative evaluations of this are relatively scarce. In this study, we measured the strength and form of sexual selection acting on a suite of male morphological traits in a wild ambush bug (Phymata americana) population at 10 sampling dates over 2 years. We tested the prediction that the strength and direction of sexual selection would be associated with one or more important ecological variables. We found that patterns of multivariate selection varied considerably over time, and even within a season. Yet, for this population, a sexually dimorphic color pattern trait was consistently a target of directional selection. The strength of sexual selection on this trait was related to both sex ratio and density, which is consistent with the idea that ecological factors can play an important role in generating patterns of sexual selection. We also demonstrate that the median strength of linear selection obtained from replicated cross-sectional methods was qualitatively similar to the estimates obtained from longitudinal methods, providing multiple lines of evidence that the evolution of sexual color dimorphism in this species is attributable to sexual selection.