Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish

Abstract

Variability in the density of groups within a patchy environment lead to differences in interaction rates, growth dynamics and social organization. In protogynous hermaphrodites there are hypothesised trade-offs among sex-specific growth, reproductive output and mortality. When differences in density lead to changes to social organization the link between growth and the timing of sex-change is predicted to change. The present study explores this prediction by comparing the social organisation and sex-specific growth of two populations of a protogynous tropical wrasse, Halichoeres miniatus, which differ in density. At a low density population a strict harem structure was found, where males maintained a tight monopoly of access and spawning rights to females. In contrast, at a high density population a loosely organised system prevailed, where females could move throughout multiple male territories. Otolith microstructure revealed the species to be annual and deposit an otolith check associated with sex-change. Growth trajectories suggested that individuals that later became males in both populations underwent a growth acceleration at sex-change. Moreover, in the high density population, individuals that later became males were those individuals that had the largest otolith size at hatching and consistently deposited larger increments throughout early larval, juvenile and female life. This study demonstrates that previous growth history and growth rate changes associated with sex change can be responsible for the sexual dimorphism typically found in sex-changing species, and that the relative importance of these may be socially constrained.

Figure 1. Comparison of sex-related size and age distributions.

Size (a, c) and age (b, d) distributions for two populations of Halichoeres miniatus at Orpheus Island (a, b) and Lizard Island (c, d). Females are shown as white bars and males as grey.

Figure 2. Comparison of areas of regular use between sexes and locations.

Mean areas of regular use for male and female Halichoeres miniatus (± SE) for Orpheus Island (grey bars) and Lizard Island (white bars) sampling locations (n = 7, except 6 females at Orpheus Island).

Figure 3. Comparison of males and female encounter rates between locations.

Frequency of encounters per minute (± SE) for Halichoeres miniatus at Orpheus Island (grey) and Lizard Island (white) sampling locations. Based on the 15 min observations of 7 males and 7 females at each location.

Figure 4. Growth of males and females by location.

Comparison of mean daily increment widths of male (i.e. females that changed sex to males; black) and female (i.e. non-sex changing fish; grey) Halichoeres miniatus collected from (a) Orpheus Island (n = 18 males, 48 females) (b) and Lizard Island (n = 16 males, 23 females). Mean standard errors are inset.

Figure 5. Changes in male growth at sex change.

Comparison of mean (± SE) otolith increment width (microns) profiles of males Halichoeres miniatus centred on the check-mark associated with sexual transition for fish collected from (a) Orpheus Island (n = 18) and (b) and Lizard Island (n = 16).

Figure 6. Size and age at sex change.

Frequency distributions of age (a, b) and standard length (c, d) at sex-change to males (determined from check marks) compared to the distributions of male Halichoeres miniatus at collection from (a, c) Orpheus Island and (b, d) Lizard Island. Age and size distributions of males at collection shown in grey, while age and back-calculated size distributions at sex change (from the otolith check marks) are displayed in white.