Reproduction of the inshore coral trout Plectropomus maculates (Perciformes: Serranidae) from the Central Great Barrier Reef, Australia

The reproductive biology of the serranid fish Plectropomus maculatus sampled from inshore waters of the Central Great Barrier Reef was studied based on histological analyses of gonad material. This species was shown to be a monandric protogynous hermaphrodite. The process of sex change foliowed the spawning period observed during September through November. Plectropomus: maculatus showed multiple spawning during this period. Sex change followed the usual protogynous mode with degeneration of ovarian germinal tissue accompanied by proliferation of male germinal tissue in the gonad. The sex structure of the sampled population was analysed based on age and size information. The size and age of first reproduction for females was 30.0cm s. L. and 2 years of age. The size and age of sex-transition was 35.4 cm s. L. and 4.4 years of age. The sex/size and sex/age relationships indicated that sex-change can occur over a broad range of sizes and ages. The sizes and age distributions of males and females P. maculates overlapped over 38% of the length range and over 42% of the maximum age observed.     

Size, maturation and the social control of sex reversal in the coral reef fish Anthais squamipinnis

A major hypothesis to explain the causal initiation of protogynous sex reversal is that females change sex upon reaching a critical size. A study of the coral reef fish Anthias squamipinnis shows that the size hypothesis does not hold. Females from two neighbouring, but spatially discrete and probably genetically homogeneous populations on Aldabra Island changed sex at distinctly different sizes. Previous laboratory and field studies in which sex reversal has followed the removal of a male from social groups have been uncontrolled and thus permit the interpretation that sex reversal is caused by non-specific social disruption or by causes other than male removal. In this study, a male was removed from each of eleven single-male and five multi-male social groups in the laboratory ( N = 8 male removals) and in the field ( N = 19 male removals). In each group, the result was that one female changed sex. Laboratory controls made it unlikely that sex reversal was induced by non-specific disruption and field observations showed that sex reversals resulted from male removals and were not coincidental, ongoing events. Previous statements that sex change is controlled by the presence or absence of a male, by inhibition of a female's tendency to change sex, or by aggression or dominance are shown, by an analysis of the complexity of issues, to be premature. Gonadal histology on 130 specimens confirmed that this species is a monandric, protogynous hermaphrodite and provided details of gonadal transformation.     

Reversed Sex Change in The Haremic Protogynous Hawkfish Cirrhitichthys falco in Natural Conditions

Bi‐directional sex change has recently been reported in a range of reef fishes, including haremic species that were earlier thought to be protogynous (female to male). However, the occurrence of this phenomenon and the social conditions driving the reversion of males to females (reversed sex change) have been poorly documented under natural conditions. Reversed sex change is predicted to occur in low‐density populations where facultative monogamy is common. However, few studies have evaluated this over a long period in such populations. We documented the occurrence of bi‐directional sex change during a 3‐yr demographic survey of a population characterised by small harem sizes in haremic hawkfish Cirrhitichthys falco. New males were derived following a change in sex of functional females (secondary males; n = 3) and juveniles always matured first as females (n = 3). Thus, C. falco exhibited a typical protogynous sexual pattern, consistent with a range of haremic fish species. We observed reversed sex change in two males. In both cases, all the females disappeared from their harems and the neighbouring males expanded their territories to encompass the territories of the sex changers. However, bachelor males did not always revert to females. A dominant male experienced bachelor status twice but regained mating opportunities following the immigration of a female into his territory or by taking a female from a neighbouring harem. Thus, we conclude that bachelor males use reversed sex change as a facultative tactic to regain reproductive status in a haremic mating system. In addition, we discuss the influence of harem size upon occurrence of reversed sex change.     

Does gonad structure reflect sexual pattern in all gobiid fishes?

Synopsis In immature and adult females of protogynous gobies, small distinctive masses of cells associated with the ovarian wall develop into testis-associated glandular structures during sex change. These precursive accessory gonadal structures, or pAGS, have been found in females of known protogynous goby species, but not among gonochoric goby species, suggesting that their presence can be used as a species-specific indicator of protogyny within the family. However, a detailed examination of a developmental series of ovaries in two gonochoric species,Gobiosoma illecebrosum andG. saucrum, revealed the presence of a gonadal feature previously thought to be restricted to protogynous gobies. Among immature females of both species, pAGS-like structures having a similar appearance and placement as functional pAGS of protogynous gobies were found. In femaleG. illecebrosum, the size of these structures among immatures progressively decreased with maturation and were absent in all but the smallest adult females. A similar pattern was evident in a small sample ofG. saucrum. Population demography based on field collections showed thatG. illecebrosum exhibits sex ratios and male and female size-frequency distributions typical of gonochores and laboratory experiments indicated that final sexual identity was unaffected by social environment during the juvenile period. Thus, the presence of pAGS in juvenile femaleG. illecebrosum is not related to an ability to change sex at that ontogenic interval. Whether the transient pAGS observed here are vestiges of an ancestral protogynous condition is unknown. Based on their presence among immatures in two gonochore gobies, however, only the presence of pAGS in adult females should be used to predict protogyny among gobies.     

Morphological ontogeny of the gonad of three plectropomid species through sex differentiation and transition

The gonadal ontogeny through sex differentiation and transition of three protogynous coral trout species, Plectropomus leopardus , P. maculatus and P. laevis was described, based on anatomical and germinal differences along the length of the reproductive tract. Gonads of immature and mature females, sex changing individuals (transitionals) and males were examined. Specific anatomical features that were compared between sexual phases included the presence and structure of sperm sinuses, gonadal musculature and germinal cell types. All three coral trout species first differentiated as an immature female. The sexual pattern of P. leopardus and P. maculatus was concluded to be diandric protogynous hermaphroditism (males were derived from the juvenile phase as well as through sex change of mature females). Plectropomus laevis was found to be monandric as males were only derived through sex change in mature females. Structural changes did not occur concomitantly with the germinal changes associated with sex change in these Plectropomus species, which is atypical for protogynous species described to date. Precursory sperm sinuses in the dorso-medial region of the gonad were present, although non-functional, in a proportion of immature and mature females of all three species. These proportions, however, varied between species depending on the sexual pattern. The structural and germinal changes observed were hypothesized as anatomical adaptations that aid in minimizing time spent in the (non-reproductive) sexual transition phase and maximizing flexibility in male development in the diandric species.     

Sex ratios and hermaphroditism in nemipterid fish from northern Australia

Of 13 nemipterid species from coastal waters around northern Australia, nine show size-related differences in sex ratio with males predominating at larger sizes. Histological examination of gonads shows that in Scolopsis monogramma S. taeniopterus and S. bilineatus this size-related skew in sex ratio results from protogynous hermaphroditism and not from sexually differentiated growth rates as has been reported for other nemipterid species. There is also evidence that, in two other species, Nemipterus peronii and Pentapodus porosus , hermaphroditism may occur. Although the mechanism by which the gonads are transformed in S monogramma and S. taeniopterus differ markedly, there is evidence to suggest that in both species sex change is a post spawning event, successful initiation of which may require females to have achieved an advanced stage of vitellogenisis.     

Comparisons of body sizes at sexual maturity and at sex change in the parrotfishes of Hawaii: input needed for management regulations and stock assessments

First estimates of sex allocation patterns and body size‐at‐sexual maturity and at protogynous sex change are presented for the five major (including one endemic) species of parrotfishes of Hawaii. Median body size at initial maturation as a female (L_M50) and at protogynous sex change from adult female to adult male (L_Δ50) varied greatly among the five species. Estimates of L_M50 were about 14, 17, 24, 34 and 35 cm fork length (L_F) in palenose Scarus psittacus, Pacific bullethead Chlorurus spilurus, stareye Calotomus carolinus, spectacled Chlorurus perspicillatus and redlip parrotfish Scarus rubroviolaceus. Values of L_Δ50 were c. 23, 27, 37, 46 and 47 cm L_F in the respective species. Length at female maturation was proportional to maximum body size (L_max) of the respective species, ranging from 50 to 72% and averaging 62% of L_max across species. L_Δ50 was also proportional to L_max, ranging from 82 to 97% and averaging 92%. Males of both pairs of Scarus and Chlorurus spp. reported here are diandric. Only one of the five major species (C. carolinus) is functionally monandric, with either all or nearly all males secondarily derived from adult females. The broadly differing absolute body sizes at sexual maturation and at sex change among the five species have important implications for improving regulatory size limits for parrotfishes in the State of Hawaii, where parrotfish species have historically been managed based on a single minimum size limit of 30·5 cm L_F. This study provides a model demonstration of why catch data for parrotfishes, and other size‐structured reef‐fish populations, should be recorded either by species or by functional size‐groups of species that allow setting more meaningful minimum size limits.     

A Review of Size at Maturity in Male Tanner (Chionoecetes bairdi) and King (Paralithodes camtschaticus) Crabs and the Methods Used to Determine Maturity

This paper reviews existing studies on the size of sexual maturityfor male Tanner or snow crab (Chionoecetes bairdi), a brachyuran,and the anomuran red king crab (Paralithodes camtschaticus).In this report the term sexual maturity is denned as the abilityto reproduce. A variety of indirect and direct methods thathave been used to determine maturity are reviewed. Examiningthe vas deferens for the presence of spermatophores was usefulin determining the size at which males first become mature.Breeding experiments in the laboratory demonstrated that mostmales, from both species, that produced spermatophores couldbreed with soft-shelled mates. Males of both species can breedat smaller sizes than do females. Morphometric techniques basedon reproductive tract weights and chela morphometry overestimatedthe sizes at which males mature in both species. Previous experimentsfor Tanner crab, which have internal fertilization, suggestsmall mature males can fertilize two to five females. Breedingexperiments showed recently matured red king crab do not appearto be able to fertilize more than one female per breeding season,while males nearing harvestable size can fertilize more thanone female. Breeding experiments and in situ observations of grasping pairsappear to be the most feasible methods for identifying malesize at maturity for these species. The value of morphometricestimations for determining when males mature is questionable.     

Allometry of sexual size dimorphism in dioecious plants: do plants obey Rensch's rule?

Rensch's rule refers to a pattern in sexual size dimorphism (SSD) in which SSD decreases with body size when females are the larger sex and increases with body size when males are the larger sex. Many animal taxa conform to Rensch's rule, but it has yet to be investigated in plants. Using herbarium collections from New Zealand, we characterized the size of leaves and stems of 297 individuals from 38 dioecious plant species belonging to three distantly related phylogenetic lineages. Statistical comparisons of leaf sizes between males and females showed evidence for Rensch's rule in two of the three lineages, indicating SSD decreases with leaf size when females produce larger leaves and increases with leaf size when males produce larger leaves. A similar pattern in SSD was observed for stem sizes. However, in this instance, females of small-stemmed species produced much larger stems than did males, but as stem sizes increased, SSD often disappeared. We hypothesize that sexual dimorphism in stem sizes results from selection for larger stems in females, which must provide mechanical support for seeds, fruits, and dispersal vectors, and that scaling relationships in leaf sizes result from correlated evolution with stem sizes. The overall results suggest that selection for larger female stem sizes to support the weight of offspring can give rise to Rensch's rule in dioecious plants.     

Gonadal development and an indication of functional protogyny in the Indian damselfish (Dascyllus carneus)

The objective of this study was to determine the sexual pattern of the Indian dascyllus Dascyllus carneus . After an initially undifferentiated state, gonads of D. carneus developed an ovarian lumen and primary growth stage oocytes, and subsequently cortical-alveolus stage oocytes. From ovaries with cortical-alveolus stage oocytes and from more developed ovaries, some gonads redifferentiated into testes. From a sample of 163 individuals, two had a gonad containing degenerating vitellogenic oocytes and proliferating spermatogenic tissue, nine had a gonad containing degenerating cortical-alveolus stage oocytes and spermatogenic tissue, and five had a gonad with degenerating primary growth stage oocytes and spermatogenic tissue. The size of these individuals overlapped greatly with the size range of mature females, suggesting that at least in some individuals, redifferentiation toward a testis occurred after spawning as females. This indicates that D. carneus is a functional, diandric protogynous hermaphrodite. Removal of a dominant male(s) did not induce a sex change in any of the ranking females in the laboratory and field groups. There was no difference in the number of chases and signal jumps performed by the ranking female between control and experimental field groups, or before and after removal of the male. However, the sizes of the ranking females were at or beyond the size range of individuals with a mixed-stage gonad, suggesting that the developmental window for female-to-male sex change may not be open ended. In 41 of 43 field groups, in which sex of fish was determined histologically or by the shape of the urogenital papilla, one to several highest size ranks were occupied by males, followed by one to several females. Mature males, however, were not limited to the highest ranks and occurred at various lower size ranks within groups. Individuals with a mixed-stage gonad also occupied various size ranks within groups.     

Socially controlled sex-change in the half-moon grouper,Epinephelus rivulatus,at Ningaloo Reef,Western Australia

The cues controlling sex-change have been elucidated for various species of hermaphroditic fishes that inhabit coral reefs, but not for the epinepheline serranids. A male removal experiment conducted on an assemblage of the half-moon grouper, Epinephelus rivulatus, demonstrated that protogynous sex-change in this species is socially controlled, possibly by the suppressive dominance of males and a threshold sex ratio. The experiment showed that a reproductively ripe female can change sex and become a male with ripening testis within 3 weeks. However, this process can be delayed, slowed, or stopped by the presence of other males in the area.     

Seasonal changes in sex ratio and size‐related sex reversal of the protogynous hermaphroditic bluespotted seabass Cephalopholis taeniops (Valenciennes, 1828)

Seasonal changes in sex ratio and size‐related sex reversal of the protogynous hermaphroditic Cephalopholis taeniops were studied from histological and population data of 218 individuals captured by hook and line, July 2009–November 2012, in Cape Verde archipelago. This study showed that C. taeniops have a diandric protogynous hermaphrodite sexual model, with young individuals undergoing bisexual development and hermaphrodites above 28 cm. All gonads had a bisexual immature stage with primary and secondary males. Primary males possibly originate from immature bisexual individuals, whereas secondary males likely result from females that have already reproduced and changed sex.     

Ecological context and the importance of body and gnathopod size for pairing success in two amphipod ecomorphs

Ecological context generates interspecific variation in mating behavior by imposing differential constraints on the action of sexual selection, but operation of these constraints in nature is not well understood. We used field and laboratory studies to examine the importance of body size and size of sexually dimorphic appendages, the gnathopods, for pairing success in two freshwater amphipod species within the Hyalella azteca species complex. We focused on a large-bodied species found in habitats where ecological factors tend to favor large body size, and a small-bodied species in habitats where small body size is favored by size-selective predation. A field study indicated that although male pairing success was greater for larger males in both species, pairing success increased throughout the range of variation in male size in the large species, whereas, in the small species, pairing success was low for smaller individuals, but roughly constant across intermediate to larger sizes. A laboratory mate choice experiment was consistent with the field study, finding that females of the large species exhibited a preference for larger males that was independent of absolute male size, but females of the small species were indifferent when choosing between males of intermediate to larger size. Species also differed in the direction of sexual size dimorphism in the field, with males being the larger sex in the large species but the smaller sex in the small species, a pattern consistent with the species differences in mate preference. Large gnathopod size relative to body size was associated with enhanced pairing success across all body sizes for the large species, but, in the small species, large gnathopod size enhanced pairing success only in smaller males. Species differences in mating behavior appear consistent with change driven by differing forms of the interaction between sexual and natural selection.     

Sex-ratio evolution in sex changing animals

Sex allocation theory is often able to make clear predictions about when individuals should facultatively adjust their offspring sex ratio (proportion male) in response to local conditions, but not the consequences for the overall population sex ratio. A notable exception to this is in sex changing organisms, where theory predicts that: (1) organisms should have a sex ratio biased toward the "first" sex: (2) the bias should be less extreme in partially sex changing organisms, where a proportion of the "second" sex matures directly from the juvenile stage; and (3) the sex ratio should be more biased in protogynous (female first) than in protandrous (male first) species. We tested these predictions with a comparative study using data from 121 sex changing animal species spanning five phyla, covering fish, arthropods, echinoderms, molluscs, and annelid worms. We found support for the first and third predictions across all species. The second prediction was supported within the protogynous species (mainly fish), but not the protandrous species (mainly invertebrates).     

Mating system and size advantage of male mating in the protogynous swamp eel Monopterus albus with paternal care

In fish with paternal care, protogynous sex change (female to male) is rare and has only been reported from species with haremic polygyny. The swamp eel, Monopterus albus, is a protogynous fish with paternal care, but little is known about its mating system. To understand protogyny in this species, we examined the mating system and male size advantage in mating in M. albus under semi-natural condition. Females swam over wide ranges and visited multiple male nests. Males defended a narrow territory around nests against other males that approached nests; at these nests, males courted and accepted visiting females. After spawning inside nests, caring males continued to perform courtship activities, and multiple breeding was observed. These observations suggest that the M. albus mating system is male-territory-visiting (MTV)-polygamy. Larger males had nests, and mated more frequently compared with small males. Because small initial males of this species are not found in nature, and because M. albus does not engage in sneaking tactics, larger nesting males do not suffer from reproductive parasitism. Thus, protogyny in this fish is likely consistent with the predictions of the size-advantage model. Biting attacks by territorial males of this predatory fish seriously wounded intruding males, occasionally resulting in the death of the intruder. We discuss the possibility that sexual differences in mortality rates in small fish may facilitate the evolution of protogyny in this species. Protogyny of the swamp eel is, to our knowledge, the first example of an MTV-polygamous mating system in a fish with paternal care.     

Sex change of primary males in a diandric labrid Halichoeres trimaculatus: coexistence of protandry and protogyny within a species

In the threespot wrasse Halichoeres trimaculatus , sex change of primary males was observed in the field and confirmed by aquarium experiments. In other words, protandry and protogyny coexisted within this species. Moreover, male-to-female-to-male sex change and female-to-male-to-female sex change were observed in aquarium experiments; i.e . reversed sex change occurred in both protandrous and protogynous hermaphrodites. These results suggest that only the direction of sex differentiation before maturation may differ between the two sexual types that have been regarded as a primary male and a protogynous hermaphrodite.     

Superparasitism and sex ratio adjustment in a wasp parasitoid: results at variance with Local Mate Competition?

Anaphes nitens is a solitary parasitoid of the egg capsules of the Eucalyptus snout beetle, Gonipterus scutellatus. Some traits of its natural history suggest that Local Mate Competition (LMC) could account for sex ratio adjustment in this species. We tested whether males emerged early, a prerequisite for fully local mating, and investigated the occurrence and effect of superparasitism on adult size and pre-emergence mortality, factors that might influence sex ratio adjustment. We found in field-collected egg capsules that males emerged first. To investigate the effects of superparasitism on adult size, we compared the sizes of parasitoids that emerged early and late from egg capsules collected in the field, and from egg capsules parasitized and superparasitized in the laboratory. Superparasitism reduced parasitoid size, affecting females more strongly than males, and increased pre-emergence mortality. We estimated A. nitens sex ratio and parasitism rate in the field during 2 years in five localities and during 4 years in a sixth. Following LMC we expected an increase in sex ratio (proportion of males) with increasing parasitism rate (assumed to reflect parasitoid density). We found that sex ratio decreased from 0.38 when the parasitism rate was low (0-20%) to 0.21 when parasitism was high (80-100%). In contrast with field results, a laboratory experiment showed that: (1) at a low parasitism level sex ratio was clearly female biased (0.28+/-0.04), (2) at a high parasitism level sex ratio increased (0.40+/-0.07), (3) male larval survivorship was not lower than female survivorship, and (4) low-quality hosts (i.e. superparasitized) were allocated more males. We conclude that LMC cannot explain the sex ratio adjustment observed in the field, even at low parasitism rates, and alternative explications for highly female-biased sex ratios must be found. One such alternative is female-biased dispersal.     

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.     

Sperm competition and sex change: a comparative analysis across fishes

Current theory to explain the adaptive significance of sex change over gonochorism predicts that female-first sex change could be adaptive when relative reproductive success increases at a faster rate with body size for males than for females. A faster rate of reproductive gain with body size can occur if larger males are more effective in controlling females and excluding competitors from fertilizations. The most simple consequence of this theoretical scenario, based on sexual allocation theory, is that natural breeding sex ratios are expected to be female biased in female-first sex changers, because average male fecundity will exceed that of females. A second prediction is that the intensity of sperm competition is expected to be lower in female-first sex-changing species because larger males should be able to more completely monopolize females and therefore reduce male-male competition during spawning. Relative testis size has been shown to be an indicator of the level of sperm competition, so we use this metric to examine evolutionary responses to selection from postcopulatory male-male competition. We used data from 116 comparable female-first sex-changing and nonhermaphroditic (gonochoristic) fish species to test these two predictions. In addition to cross-species analyses we also controlled for potential phylogenetic nonindependence by analyzing independent contrasts. As expected, breeding sex ratios were significantly more female biased in female-first sex-changing than nonhermaphroditic taxa. In addition, males in female-first sex changers had significantly smaller relative testis sizes that were one-fifth the size of those of nonhermaphroditic species, revealing a new evolutionary correlate of female-first sex change. These results, which are based on data from a wide range of taxa and across the same body-size range for either mode of reproduction, provide direct empirical support for current evolutionary theories regarding the benefits of female-first sex change.     

Fitness and body size in mature odonates

The relationship between body size and fitness components in odonates was examined using a meta‐analysis of 33 published studies. There was a positive and significant overall effect of body size on mating rate and lifetime mating success among males. There was also a weaker but still significant positive effect of body size on survivorship of males. The relationship between body size, mating rate, longevity, and lifetime mating success differed significantly between males of territorial and nonterritorial species. The effect of body size was significant for all fitness components in territorial species but significant only for longevity and lifetime mating success in nonterritorial species. Effect sizes appeared to be strongest on longevity in both sexes, and on male mating rate in territorial species. Other effect sizes, even when significant, were small. Despite a much smaller data set, female fitness also increased significantly with body size. Both clutch size and longevity showed a significant positive relationship with body size. These results suggest that there is a general fitness benefit to large size in odonates. Nevertheless, significant heterogeneity is apparent in this effect, which can be attributed to sex, mating system, and fitness component. Finally, these analyses point to inadequacies in the current data that need further study before the potentially rich patterns in size effects on fitness can be explored more thoroughly.