Douglas Y. Shapiro

Sperm Economy in a Coral Reef Fish, Thalassoma Bifasciatum

In many coral reef fishes, males face the evolutionary problems of how to allocate sperm among frequent, daily mating in order to maximize the number of eggs they fertilize. A method is developed and tested for collecting and counting the number of sperm and eggs released during separate spawns of the coral reef fish Thalassoma bifasciatum. The method was used to examine the pattern of sperm allocation for pair— and group—spawning males. The number of sperm released by pair—spawning males varied positively with the number of eggs released by their female mates and with female body size. The data suggest that males economize on sperm release by providing the minimum amount of sperm needed to fertilize the egg clutch of the female partner. Fertilization efficiency (the number of eggs fertilized by a given number of sperm) was higher with large females than it was with small females. Males differed significantly among themselves in sperm output per spawn, with some males consistently releasing more sperm than other males with same—sized females. Male—male differences were not due to differences in male body size, quality of the spawning site, or the apparent degree of water movement. The number of sperm released per spawn did not decline throughout the daily spawning period, a pattern that disproved one but not all possible patterns of sperm depletion. In group spawns, the total number of sperm released and the number released per male were respectively 50 and 6 times the number released in pair spawns, on average. Both of these measures increased significantly with the clutch size of the spawning female. Overall, sperm production is probably sufficiently costly that males have been selected to allocate sperm carefully among their frequent daily spawns.

Social Behavior, Group Structure, and the Control of Sex Reversal in Hermaphroditic Fish

Publisher Summary This chapter describes the phenomena of protogynous sex reversal and discusses the mechanisms that control its initiation and completion. It relates these processes to the spatial structure and composition of social groups. The social and developmental hypotheses for the control of sex reversal are examined and a new hypothesis is proposed: females are stimulated to change sex by the changes in a specific behavioral measure of a critical magnitude. The control of sex reversal and its relation to social systems has been confined to a few species. Emphasis is given on Anfhius squarnipinnis. A. squarnipinnis is a small, sexually dimorphic fish that occupies stable, sedentary social groups in the shallow water around coral reefs. The social groups are of variable size and composition, ranging from small, single-male groups to groups containing 35 males and more than 350 females. Some groups are subdivided into two or three spatially separated subgroups. The chapter describes the process by which a group becomes subdivided is closely related to the control of sex reversal.

Serial female sex changes after simultaneous removal of males from social groups of a coral reef fish.

The simultaneous removal of three to nine males from large social groups of Anthias squamipinnis led to close to a one-to-one replacement of the removed males by sex-reversing females. The females changed sex serially within each group with a mean interval between successive onset times of 1.9 days. The timing of sex change is thus not independent for each fish but is influenced by the events surrounding other sex reversals within the group.

Pelagic spawning and egg transport in coral-reef fishes: a skeptical overview

The literature on the pelagic spawning of inshore reef fishes is replete with the idea that individuals spawn at times and specific locations that ensure eggs being swept quickly off reefs and into offshore waters. The choice of spawning times and sites has been hypothesized to function primarily either to minimize egg predation from reef-associated fishes and invertebrates (Johannes 1978), to maximize dispersal (Barlow 1981), or to provide maximum opportunity for pelagic larvae to survive in waters with patchy and irregular distribution of food (Doherty et al. 1985). All of these ideas share two assumptions: that it is advantageous for pelagic eggs and/or larvae to be removed from shallow reefs as quickly as possible, and that this advantage has acted as a selective force to produce specific spawning times and sites. Several behavioral strategies resulting from this selective pressure have been proposed (Randall & Randall 1963, Jones 1968, Ehrlich 1975, Warner et al. 1975, Johannes 1978, Robertson 1983): (1) migrating to the edge of the insular shelf to spawn; (2) spawning at the outer or downstream edges of reefs; (3) spawning from local promontories high in the water column or ejecting gametes at the top of a spawning rush; and (4) spawning during strong local off-reef or offshore currents, e.g. during spring

Group sex ratio and sex reversal

Abstract In hermaphroditic fishes, the initiation of sex reversal by male removal explains the replacement of lost males but does not explain how the number of males in a group may increase. Since numerous species apparently cannot produce primary males, a second means of initiating sex reversal must exist. In the present study we formulate a model which suggests the existence of an additional mechanism governing sex change: as soon as the ratio of adult females to males within a group exceeds a certain threshold value, a female changes sex even though no male has been removed. This process is inferred from comparison of data collected in the Red Sea and the western Indian Ocean with the models predictions concerning size at sex reversal and the sex ratio of groups. The results suggest how several ecological factors may influence the occurrence rate of sex reversal and the development and growth of social groups.

Behavioral influences on gene structure and other new ideas concerning sex change in fishes

SynopsisThe interpretation of experiments, designed to reveal whether sex change is induced behaviorally, can influence the type of physiological mechanism we propose to underlie sex change. Mechanisms involving stimulation differ from mechanisms of disinhibition and each is inferred from different ways of conceptualizing behavioral experiments. Both types of mechanism are likely to involve CNS, hypothalamus, pituitary, and gonad. Recent work, however, also implicates H-Y antigen and Bkm satellite DNA in the sex-change process. These studies raise the exciting possibility that the changes in behavioral relationships between the sexes that induce sex change also produce changes in certain aspects of DNA. The nature of the proximate causes of sex change plays a surprisingly important role in influencing evolutionary models of sex change. Such models can be evaluated by first examining their applicability to real populations and, if they are applicable, then testing their validity by comparing their predictions with observed data. The size advantage model, in spite of its proven ability to stimulate and direct research, does not fare well in either of these stages of evaluation. The basic weakness of the model is its failure to incorporate individual adaptability into the life history of sex-changing fishes.

Social faciliation and sensory mediation of adult sex change in a cryptic, benthic marine goby

When females of the protogynous gobiid, Coryphopterus glaucofraenum Gill 1863, were removed from their natural social system and isolated from males in all-female groups, the number of females in a group influenced both the proportion of groups exhibiting sex change, as well as the number of females changing sex within groups. Sex change was most prevalent in large, all-female groups; solitary females, however, infrequently changed sex. Therefore, in C. glaucofraenum the presence of other female conspecifics promotes sex change. In the presence of larger male(s), the incidence of sex change among experimental females was either reduced or negated, depending upon the number of females. Sensory isolation experiments revealed the importance of two sensory modalities in the induction and incidence of sex change. Water-borne cues, probably chemical in nature, released by conspecific female groups increased the probability of sex change among solitary females. These induction cues were both sex- and species-specific. In addition, visual cues influenced the number of females changing sex within larger, all-female groups. Visual cues, in the absence of other means of information exchange, appear to play a role in determination of group membership among female C. glaucofraenum. Lastly, while all females within social groups experienced the same sensory cues, usually only the largest female(s) ultimately changed sex. Thus, while sensory cues mediated the timing of sex change, other factors (probably social) likely played a part in determining which individuals within the social group actually changed sex.

Distinguishing behavioral interactions from visual cues as causes of adult sex change in a coral reef fish

Two experiments tested the hypothesis that adult female-to-male sex reversal in protogynous fish is induced by the loss of close-contact behavioral interactions between males and females, and not by the loss of simple visual cues from the male. Twenty-six laboratory groups of Anthias squamipinnis were manipulated so that females within each group (1) retained chemical and acoustic access to a male, (2) were denied behavioral access to a male, and (3) were either allowed or denied visual access to a male alone or to a male interacting with another female. At least one female subsequently changed sex in each of 22 groups. While acoustic and chemical cues were not completely eliminated as possible causes, sex change is apparently induced by loss of male-female behavioral interaction in combination with continued interaction between females.

The influence of females on the initiation of female-to-male sex change in a coral reef fish

Abstract In the protogynous coral reef fish Anthias squamipinnis (Peters), all males are sex-reversed females. A sexually mature female can be induced to change sex by removing a male from her social group. The influence of non-sex-changing females on the initiation of sex change was evaluated in 109 social groups in the Gulf of Eilat. When the male and largest female were removed from each of 12 single-male groups, the second-largest female changed sex in 9 groups. This result distinguished between two behavioral hypotheses suggested by previous work and made it tenable that a particular behavioral measure, the profile of behavior-received, that depends on adult females, is critical to the initiation of sex change. This species forms all-female groups as well as bisexual groups. All-female groups can be expected to have some mechanism for the production of a male. The removal of the largest female from each of 8 all-female groups failed to induce sex change in any group. The dominant female in these groups thus does not function in the same way as does the male in bisexual groups, at least in terms of the initiation of sex change. Following the removal of the male from each of 8 bisexual groups containing five or fewer adult females, a female changed sex in only 4 groups. This 50% incidence of sex reversal was lower than the 77–80% incidence in control groups containing more than five adult females. Data suggest that a minimum of four adult females is probably required for the probability of sex change after male removal to equal 75%.

Bisexual juvenile gonad and gonochorism in the fairy basslet, Gramma loreto

According to sex allocation theory, protogynous species ought to form social systems in which a relatively small number of males mate with a relatively large number of females. Because the fairy basslet, Gramma loreto, mates in this predicted manner, we examined its mode of sexuality, looking for evidence of protogyny, in 167 specimens ranging in size from small juveniles through adults. All gonads initially developed previtellogenic oocytes and a precursor of the sperm ducts. In future males, the oocytes degenerated; the ducts proliferated, anastomosed, and became available for sperm transport; and spermatogenic tissue appeared. In future females, an ovarian lumen was formed, the precursive sperm ducts degenerated, and oocytes continued to grow. No histological features indicative of protogyny were found. In an experimental attempt to induce sex reversal, males were removed from social groups transferred from natural populations into the laboratory. Five months after male removal, no female contained any histological evidence of sex change. Thus, our data strongly support the hypothesis that G. loreto is a gonochore. The species does not conform to the predicted relationship between protogyny and a femalebiased mating system, perhaps because small, nonreproductive males evolved an alternative means of avoiding low reproductive success by growing faster than similarly sized females.