A male poecillid's sexually dimorphic body plan, behavior, and nervous system

Here we review the literature of a male poecillid's sexually dimorphic body plan, behavior, and nervous system, including work dating from the mid 1800s to the mid 1990s as well as work in press or in preparation for publication. Rosa-Molinar described the remodeling of the sexually dimorphic anal fin appendicular support, confirmed earlier claims about the development of the male and female secondary sex characteristics in the Western Mosquitofish, Gambusia affinis and provided for the first time direct embryonic evidence suggesting that remodeling of the sexually dimorphic anal fin appendicular support is biphasic. The first process begins in embryos and proceeds similarly in immature males and females; the second process occurs only in males and results in the anterior transposition of the anal fin and its appendicular support to the level of vertebra 11 [Rosa-Molinar E, Hendricks SE, Rodriguez-Sierra JF, Fritzsch B. 1994. Development of the anal fin appendicular support in the western mosquitofish, Gambusia affinis (Baird and Girard, 1854): a reinvestigation and reinterpretation. Acta Anat 151:20-35.] and the formation of a gonopodium used for internal fertilization. Studies using high-speed video cameras confirmed and extended Peden's and others' observations of copulatory behavior. The cameras showed that circumduction is a complex movement combining in a very fast sequence abduction, extension and pronation, S-start-type fast-start (defined as torque-thrust), and adduction movements. Recent work on the nervous system demonstrated dye-coupling between motor neurons and interneurons via gap junctions, suggesting an attractive substrate for the rapid motions involved in poecillid copulatory reflexes.     

Permanent and Seasonal Expressions of Sexual Dimorphisms in a Weakly Electric Fish, Mormyrus rume proboscirostris Boulenger 1898 (Mormyridae, Teleostei)

Several sexually dimorphic characters of the anal-fin complex in the mormyrid fish, Mormyrus rume proboscirostris, assist during courtship when the male envelops the female's anal fin with its own to form a common spawning pouch (anal-fin reflex). We found that developmental growth and seasonally cycling gonadal activity selectively affect their expression. The structures defining the anal fin undergo a permanent sexually dimorphic transformation at a time when ripe spermatozoa first appear in the testis of young males. However, the expression of a dorsally directed indentation of the posterior ventral body wall, affecting the dorsal margin of the anal fin, appeared to be more plastic as it correlated with the gonadosomatic index, that is, testis size. We surmised that this indentation is influenced by cyclic anabolic action on muscle involved with the execution of the anal-fin reflex.     

Sexually selected traits are larger and more variable in male than female beach-spawning capelin,Mallotus villosus

We evaluated whether morphological traits in capelin, Mallotus villosus, that appear to be sexually selected (pectoral fin, pelvic fin, anal fin, lateral ridge) were larger and more variable in males than females compared with naturally selected morphological traits (eyes, dorsal fin). Photographs were obtained of 136 capelin captured at two spawning sites and standardised measurements were taken of six morphological traits. Males had larger traits than females for a given body size and this was most pronounced in the traits thought to be sexually selected. Body size explained much of the variation in female traits but less variation in male traits, suggesting alternative selection pressures are involved. We suggest that larger male body size aids in endurance rivalry and sexually dimorphic traits help males to remain in physical contact with females while spawning on the beach.     

Development of secondary sexual characters and their relationship to ontogeny and seasonal reproductive period in Hyphessobrycon igneus (Ostariophysi: Characiformes)

Sexual dimorphism in size, anal‐fin shape and coloration of Hyphessobrycon igneus, Characidae, were examined. Males were more frequent at larger body sizes, confirming body size as a sexually dimorphic trait. Anal‐fin shape and the colour of all fins were the same for females and juveniles, differing only in adult males. Likewise, only adult males had bony hooks on fin rays; larger and more sexually mature males had the most numerous and developed hooks and hooks were most developed in degree and number during peak reproductive periods. Fin hooks regressed in number and developmental degree after the reproductive period, but restarted development with the beginning of the new reproductive period without completely disappearing. Results show that bony hooks have a development and regression cycle related to reproductive seasonality.     

New remarkable sexually dimorphic miniature species of Hyphessobrycon (Characiformes: Characidae) from the upper Rio Tapajós basin

A new miniature species of Hyphessobrycon is described from an affluent of the Rio Papagaio, tributary of the Rio Juruena, upper Rio Tapajós basin, Mato Grosso State, Brazil. The new species can be distinguished from its congeners by having a remarkable secondary sexual dimorphism in its live colouration (males are red and females yellow), well‐defined and relatively narrow dark midlateral stripe extending from tip of snout to tip of middle caudal‐fin rays, absence of humeral blotch, 15–18 branched anal‐fin rays and five or six branched pelvic‐fin rays. The sexually dimorphic colouration of the new species is briefly discussed regarding its temporal variation.     

Effects of 17α-Methyltestosterone on Sexually Dimorphic Characters in the Weakly Discharging Electric Fish,Brienomyrus niger(Günther, 1866) (Mormyridae): Electric Organ Discharge, Ventral Body Wall Indentation, and Anal-Fin Ray Bone Expansion

Adult males of African weakly discharging electric fish (family: Mormyridae) are distinguished from juveniles and adult females by a dorsally directed indentation of the posterior ventral body wall and by massive bone expansion of the bases of a select number of anal-fin rays. These sexually dimorphic structures seem to facilitate the anal-fin reflex that is displayed during courtship when the male envelopes its anal fin around the female's to form a common spawning pouch. Expanded bone could provide additional surface for muscle attachment and thus assist in part with the courtship sequence. Based on the fact that the expression of the male sexually dimorphic electric organ discharge (EOD) is under androgen control, and that the female EOD can be masculinized through testosterone administration, we hypothesized that androgens should also drive anal-fin ray bone expansion in male mormyrids and equally effect male-like changes in treated juveniles and adult females. Exogenous androgen treatment (17α-methyltestosterone) of adult femaleBrienomyrus nigerresulted in a male-like EOD, and male-typical structural transformations (body wall indentation and anal-fin ray bone expansion). Some of these changes were immediate and receded following hormone withdrawal (EOD), while others developed more slowly and were apparently permanent (indentation and bone formation). 17α-Methyltestosterone administration affected only those targets in females that are normally involved in the male's reproductive behavior, i.e., its courtship signal (EOD) and two morphological features (body-wall indentation and bone expansion). Rays of the dorsal or caudal fins were never affected.     

Among-population variation in adipose fin size parallels the expression of other secondary sexual characteristics in sockeye salmon (Oncorhynchus nerka)

The small, non-rayed adipose fin is present in eight extant orders of fishes, including the Salmoniformes (salmon and trout) but the functional significance of the trait is unknown. Recent evidence suggests a hydrodynamic function in juvenile salmonids, and observations of sexually dimorphic adipose fin expression and female preference for males with large fins indicate a role in reproduction by mature individuals. To the extent that the adipose fin functions in reproduction, it might be expected to evolve in parallel with other sexually dimorphic traits, such as body depth and jaw length. To test this hypothesis, we quantified adipose fin size of mature male sockeye salmon, Oncorhynchus nerka, among five populations. Populations differed significantly in adipose fin size after correcting for variation in body length and body depth. Adipose fin size tended to parallel the development of other secondary sexual characteristics, but was more closely related to body length and body depth than jaw length. Interestingly, shallow bodied populations from small creeks with high brown bear, Ursus arctos, predation during spawning tended to have smaller size-adjusted adipose fins than populations spawning in deeper water. However, it remains unclear whether adipose fin size is being selected independently of other traits or if it is pleoitropically linked to a trait under selection (e.g., body size or shape).     

Androgenization of Dominant Males in a Cichlid Fish: Androgens Mediate the Social Modulation of Sexually Dimorphic Traits

We present data on the relationship between social status and male secondary sex traits, both morphological and ethological, in Oreochromis mossambicus at the onset of sexual maturation. There is a differential expression of morphological (dorsal fin height, anal fin height, mandible width and premaxilla length) and behavioural (nuptial coloration, per cent time defending a territory, spawning pit volume, pit hovering and courtship rate) traits according to social status, with dominants presenting the highest expression of these dimorphic traits. Social status also affects the development of the genital papillae, which is considered to be a good predictor of androgen levels in cichlid fishes. The results support a causal model in which social status modulate androgen levels that in turn modulate the expression of behavioural and morphological male traits.     

On the threshold of dispersal: hitchhiking on a giant fly favours exaggerated male traits in a male‐dimorphic pseudoscorpion

The evolution of exaggerated male traits is frequently driven by competition between males to control resources critical for female survival and/or reproductive success. For flightless arthropods specializing on patchy habitats, dispersal agents may represent one such critical resource. The Neotropical pseudoscorpion, Semeiochernes armiger, disperses to new habitats by attaching to the giant timber fly, Pantophthalmus tabaninus, as it ecloses from pupal boreholes within decaying Ficus trees. In a study that combined field observations of mating with experimental removal of individuals from a large, pre‐dispersal population, our morphometric analyses revealed that S. armiger is among the most highly sexually dimorphic pseudoscorpions known, with males possessing unusual, triangular‐shaped pedipalpal chelae (hands) and a male‐specific, dimorphic chela peg that exhibits threshold trait expression. Several lines of evidence indicate that extreme sexual dimorphism in S. armiger results from male competition to monopolize pantophthalmid bores as strategic sites for inseminating females on the verge of dispersal. Sexually dimorphic pedipalpal characters were significantly larger in males located in and around pantophthalmid boreholes, compared with males collected at the periphery of the pantophthalmid emergence zone. Removal of pseudoscorpions resulted in a significant decline in pedipalpal size of males associated with pantophthalmid bores, followed by a rebound in size after collected individuals were returned to the tree. Most significantly, field observations of mating indicate that this competition translates into intense selection for exaggerated male traits, with all traits of the sexually dimorphic chelae exhibiting highly significant sexual selection differentials in males. © 2013 The Linnean Society of London     

Sexual Dimorphisms in the Dermal Denticles of the Lesser-Spotted Catshark,Scyliorhinus canicula (Linnaeus, 1758)

The dermal layers of several elasmobranch species have been shown to be sexually dimorphic. Generally, when this occurs the females have thicker dermal layers compared to those of males. This sexual dimorphism has been suggested to occur as a response to male biting during mating. Although male biting as a copulatory behaviour in Scyliorhinus canicula has been widely speculated to occur, only relatively recently has this behaviour been observed. Male S. canicula use their mouths to bite the female’s pectoral and caudal fins as part of their pre-copulatory behaviour and to grasp females during copulation. Previous work has shown that female S. canicula have a thicker epidermis compared to that of males. The structure of the dermal denticles in females may also differ from that of males in order to protect against male biting or to provide a greater degree of friction in order to allow the male more purchase. This study reveals that the length, width and density of the dermal denticles of mature male and female S. canicula are sexually dimorphic across the integument in areas where males have been observed to bite and wrap themselves around females (pectoral fin, area posterior to the pectoral fin, caudal fin, and pelvic girdle). No significant differences in the dermal denticle dimensions were found in other body areas examined (head, dorsal skin and caudal peduncle). Sexually dimorphic dermal denticles in mature S. canicula could be a response to male biting/wrapping as part of the copulatory process.     

Sexual dimorphism and allometry of external morphology in Oreochromis mossambicus

Sexual dimorphism in growth of conventional morphometric characters was investigated in juveniles and young adults (size range: 31 to 91 mm) of Oreochromis mossambicus . A closely associated set of traits was identified that shows sexually dimorphic growth, which was positively allometric in the males. These traits correspond to two different morphological complexes: jaw structure and anal/dorsal fins. The best sex discriminators among this set of traits were premaxilla width, anal fin height and snout length. These findings may be explained in terms of intra– and inter–sexual selection acting together and favouring males with strong and large mouths and high dorsal and anal fins, traits that are important in agonistic displays (jaw and fins), fighting and nest digging (jaw).     

Sexual dimorphism and mental barbel structure in the South Georgia plunderfish Artedidraco mirus (Perciformes: Notothenioidei: Artedidraconidae)

A recent sample (28 specimens from South Georgia and 1 from Shag Rocks) of the plunderfish Artedidraco mirus collected in June 2004 during the ICEFISH Cruise yielded sufficient data to refute two long-held assumptions about this species: (1) it is endemic to South Georgia; (2) its mental barbel is sexually dimorphic (tapered in females and club-shaped with papillae in males). A. mirus exhibits three types of mental barbel: A: tapered without a terminal expansion; B: with a narrow terminal expansion composed of simple papillae; C: with a wide terminal expansion composed of convoluted or elaborately branched papillae. There is no correlation between barbel type and body size or sex. We also found sexual dimorphism in the relative height of the second dorsal fin (30% higher on average in males) and in the colour of the anal fin (black in males over 60 mm SL). The largest males possess a prominent ruffled urogenital papilla, also black in colour. Barbel histology resembles that of other artedidraconids (Dolloidraco longedorsalis, Pogonophryne scotti) studied in containing large nerve trunks and blood vessels lateral to a pseudocartilaginous core and dermal papillae with an extensive network of nerves and blood vessels. The high degree of intraspecific variation in artedidraconid barbel structure warrants caution in using this structure as a diagnostic taxonomic character.     

Colour perception in three-spined sticklebacks: sexes are not so different after all

Sexual selection theory implies a tight coupling between the evolution of male sexual display and the sensory capabilities of the female. In sexually dimorphic species it is proposed that this might lead to sex differences in a species’ perceptive abilities. However, supporting evidence for this is rare, and to date there is only one example; three-spined sticklebacks, Gasterosteus aculeatus. Here, the female’s visual system is reported to become more red-sensitive during the summer breeding season; a time when sexually mature males display a red throat and belly to potential mates. In contrast, a shift in sensitivity is not apparent in males. These results, although commonly quoted, are surprising because previous observations suggest that both sexes may benefit from the detection of the male’s red colour patch; in females the intensity of red coloration can influence the choice of mate, and in males the conspicuous red colouration can aid the detection of rival males. To investigate this paradox we repeated the original optomotor experiment using a fully controlled design. In contrast to the earlier result, we found that both males and females exhibit a shift in their sensitivity to red during the reproductive period. These new data therefore do not support the hypothesis that sex differences in perceptual abilities occur in sexually dimorphic species.     

NATURAL SELECTION AND SEXUAL SIZE DIMORPHISM IN RED-WINGED BLACKBIRDS

Patterns of overwinter mortality in the sexually dimorphic red-winged blackbird (Agelaius phoeniceus) were examined to test the predictions of the sexual-selection hypothesis that male size is limited by directional selection favoring small males and that female size is maintained by stabilizing selection wherein extreme phenotypes experience higher mortality. Museum specimens collected from Ontario over a 95-yr period were used to compare the sizes of males and females collected in fall and spring. In a separate field study, body sizes of returning and nonreturning male and female red-winged blackbirds were compared over a 6-yr period. Overall, there was no evidence of higher overwinter mortality among larger males. Among adult (ASY) males, large individuals appeared to have higher survival than small individuals, although among subadult (SY) males, large size may have been disadvantageous. Weak evidence of stabilizing selection on female body size was found. Among adults, sexual size dimorphism seemed more pronounced after winter than before winter. Our results do not support the hypothesis that body size in male red-winged blackbirds is limited by selective mortality outside the breeding season. It is possible that size selection occurs earlier in life, when males are still in the nest. Our results suggest that caution should be exercised when interpreting interspecific evidence showing higher adult male than female mortality in sexually dimorphic species. Such patterns could arise as a cost to males of sexual selection and yet provide no insight into how natural selection opposes sexual selection for increased male size.     

A male sexually dimorphic trait provides antimicrobials to eggs in blenny fish

Predation and microbial infections are the major causes of natural mortality for early life stages of oviparous species. The parental traits reducing the effects of predation are rather well described, whereas antimicrobial mechanisms enhancing offspring survival are largely unexplored. In this paper, we report that a male sexually dimorphic trait, the anal glands, of the redlip blenny (Ophioblennius atlanticus atlanticus) and the peacock blenny (Salaria pavo), two fish species with paternal egg care, produce a mucus enriched with antimicrobial substances. Histological and histochemical analyses showed that the anal glands of these species are characterized by the massive presence of mucus-secreting cells. Anal gland extracts, from both the hydrophilic and the hydrophobic protein fraction, exhibited a lysozyme-like activity. Field observations demonstrated that redlip blenny males, while performing egg care, rub the anal region over the nest internal surface, probably facilitating the transfer of mucus to eggs. These results strongly indicate that this sexually dimorphic trait is involved in egg defence against microbial infections.     

Osteology of Paedocypris,a miniature and highly developmentally truncated fish (Teleostei: Ostariophysi: Cyprinidae)

Species of the cyprinid genus Paedocypris are among the smallest and most developmentally truncated fishes and vertebrates. Our analysis of their skeletal structure reveals a puzzling combination of extreme developmental truncation and an increased morphological complexity in sexually dimorphic characters. The skeleton of Paedocypris is characterized by reduction and loss and resembles in many aspects that of a larval/early juvenile stage of its close relatives. We found 61 characters that have been affected by developmental truncation. A comparison with the skeletal development of a close relative, the zebrafish Danio rerio, demonstrates that the majority of the absent bones or skeletal structures in Paedocypris are those that appear late in the ossification trajectory of the zebrafish. Thus, their absence in Paedocypris seems to be due to the simple developmental truncation of terminal stages in the ossification sequence. Our study of the sexually dimorphic structures in Paedocypris demonstrates that predominantly the male exhibits the more complex state. In relation to the female, male Paedocypris uniquely possess a cleithrum with a pointed posterior process that covers the scapula laterally, and a more medially situated posterior flange that contacts the dorsal area of the coracoid; a massive and heavily ossified uppermost pectoral radial tightly bound to the scapula; thickened and enlarged three uppermost pectoral‐fin rays; a large triangular, dorsolaterally directed process on the outer arm of the massive os suspensorium; and a enlarged and shovel‐like anterodorsally directed basipterygium; and a hypertrophied first pelvic‐fin ray with additional anterior flanges that support keratinized pads of skin. Female Paedocypris show only one structure that is better developed than in males: the first proximal‐middle radial and the anteriormost fin ray of the dorsal fin are more massive and more heavily ossified. Although the function and biological role of these dimorphisms is still unknown, we hypothesize that they are related to a special reproductive behavior. Paedocypris is a prime example for the recent claim that miniaturization among cyprinids is associated with evolutionary novelty only in developmentally truncated miniatures and not in proportioned dwarfs. Paedocypris offers a strong challenge to Schindleria as the most extreme example of developmental truncation known among fishes. We highlight the difficulties that developmentally truncated taxa frequently pose to the resolution of their phylogenetic position and propose an approach to overcome this problem. Our phylogenetic comparison to determine the systematic position of Paedocypris among cyprinids reveals that it shares not only a number of unique absences, but also highly unusual progressive characters with Sundadanio and Danionella, two other Asian miniature cyprinids. We hypothesize that the three genera form a monophyletic group. We further found that Paedocypris and Danionella share a number of uniquely derived characters pointing to a sister group relationship of the two. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

Ontogenetic stage‐specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations

Sexual dimorphism can evolve when males and females differ in phenotypic optima. Genetic constraints can, however, limit the evolution of sexual dimorphism. One possible constraint is derived from alleles expressed in both sexes. Because males and females share most of their genome, shared alleles with different fitness effects between sexes are faced with intralocus sexual conflict. Another potential constraint is derived from genetic correlations between developmental stages. Sexually dimorphic traits are often favoured at adult stages, but selected against as juvenile, so developmental decoupling of traits between ontogenetic stages may be necessary for the evolution of sexual dimorphism in adults. Resolving intralocus conflicts between sexes and ages is therefore a key to the evolution of age‐specific expression of sexual dimorphism. We investigated the genetic architecture of divergence in the ontogeny of sexual dimorphism between two populations of the Japanese medaka (Oryzias latipes) that differ in the magnitude of dimorphism in anal and dorsal fin length. Quantitative trait loci (QTL) mapping revealed that few QTL had consistent effects throughout ontogenetic stages and the majority of QTL change the sizes and directions of effects on fin growth rates during ontogeny. We also found that most QTL were sex‐specific, suggesting that intralocus sexual conflict is almost resolved. Our results indicate that sex‐ and age‐specific QTL enable the populations to achieve optimal developmental trajectories of sexually dimorphic traits in response to complex natural and sexual selection.     

Role of cell death in the formation of sexual dimorphism in the Drosophila central nervous system

Currently, sex differences in behavior are believed to result from sexually dimorphic neural circuits in the central nervous system (CNS). Drosophila melanogaster is a common model organism for studying the relationship between brain structure, behavior, and genes. Recent studies of sex‐specific reproductive behaviors in D. melanogaster have addressed the contribution of sexual differences in the CNS to the control of sex‐specific behaviors and the development of sexual dimorphism. For example, sexually dimorphic regions of the CNS are involved in the initiation of male courtship behavior, the generation of the courtship song, and the induction of male‐specific muscles in D. melanogaster. In this review, I discuss recent findings about the contribution of cell death to the formation of sexually dimorphic neural circuitry and the regulation of sex‐specific cell death by two sex determination factors, Fruitless and Doublesex, in Drosophila.     

Involvement of HGF/MET signaling in appendicular muscle development in cartilaginous fish

In amniotes, limb muscle precursors de-epithelialize from the ventral dermomyotome and individually migrate into limb buds. In catsharks, Scyliorhinus, fin muscle precursors are also derived from the ventral dermomyotome, but shortly after de-epithelialization, they reaggregate within the pectoral fin bud and differentiate into fin muscles. Delamination of muscle precursors has been suggested to be controlled by hepatocyte growth factor (HGF) and its tyrosine kinase receptor (MET) in amniotes. Here, we explore the possibility that HGF/MET signaling regulates the delamination of appendicular muscle precursors in embryos of the catshark Scyliorhinus canicula. Our analysis reveals that Hgf is expressed in pectoral fin buds, whereas c-Met expression in fin muscle precursors is rapidly downregulated. We propose that alteration of the duration of c-Met expression in appendicular muscle precursors might underlie the evolution of individually migrating muscle precursors, which leads to the emergence of complex appendicular muscular systems in amniotes.     

The role of the transformer genes in the development of genitalia and analia of Drosophila melanogaster

The autosomal mutations transformer (tra) and transformer-2 (tra-2) of Drosophila convert chromosomal females (X/X) into phenotypical males. Our analysis aims at an understanding of the role which the transformer genes play in the development of the sexually dimorphic genital disc. In each Drosophila embryo, this disc starts development with a male and a female genital primordium, and an anal primordium. Our experiments involved the production of cell clones that were made homozygous for tra or tra-2 at different times of development. Homozygous clones were obtained by inducing mitotic recombination in three types of females heterozygous for tra or tra-2. The cells of the homozygous tra/tra or tra-2/tra-2 clones responded by changing from the female into the male pathway. Male genital structures developed if the clones were induced not later than 81 hr into development. In the analia, male clones appeared up to 120 hr. Our results show that the action of the wild-type alleles of tra⁺ and tra-2⁺ is required until late in larval development to repress the male genital primordium and to support development of the female primordium, as well as to maintain the anal primordium in the female pathway. Our data also suggest that the embryonic genital disc consists of two compartments, one containing the precursors for penis and analia, the other those of the male and female genitalia.