The relationship between sex change and reproductive success in a protandric marine gastropod

Abstract

Protandric species switch sex during their lifetime. According to theory, the time (body size) at which sex change occurs is determined by the reproductive success of individuals affected by social interactions as well as by post-copulatory factors. Experimental evidence is biased to few social systems making the exploration of general patterns difficult. We used the protandric marine gastropod Crepidula coquimbensis that partakes in intrabrood sibling cannibalism to test the following hypotheses: 1. Male-male competition for access to females and sibling cannibalism determine male reproductive success; 2. Males with greater access to females and with higher reproductive success will have reduced growth rates and will delay sex change. Artificial aggregations with different social structures were constructed and male reproductive success was estimated by paternity analysis. The results supported our expectations showing that male competitive ability for access to the female, time spent by males in the copulatory position, and sibling cannibalism affect reproductive success and influence time to sex change, with less successful males hastening sex change. Also, males that spent more time in the copulatory position had reduced growth rates. Comparing these results with those reported for other sequential hermaphrodites provides evidence supporting general patterns of sex change in nature.

Figure 1

(a) Photographs of C. coquimbensis showing anatomical details of individuals at the male stage and transitional stage (changing from male to female). (b) One female and two males (individuals with red and blue spots) inside of a host shell of the marine gastropod Tegula sp. (c) A close up of the individuals inside the host shell. (d) Plastic boxes used to maintain the experimental aggregations of C. coquimbensis.

Figure 2. Number of C. coquimbensis males observed in the copulatory position in the treatments 1F+2M, 1F+4M.

Also, the number of males fathering the brood, estimated from paternity analysis, is presented. Estimates include two ovicapsule laying events and before and after embryonic cannibalism. Vertical lines on each bar correspond to 1 standard deviation.

Figure 3. Change in the reproductive success of C. coquimbensis males during intracapsular development as a product of embryo cannibalism.

Positive values represent an increase in participation in fathering the brood; negative values represent a decrease in participation in fathering the brood.

Figure 4. The relationship between the time spent by males in the copulatory position and male reproductive success in terms of its relative contribution to the brood measured after embryo cannibalism for C. coquimbensis.

Results for treatments 1F+2M and 1F+4M are shown.

Figure 5

(A) Growth rate (mm/day) of the first C. coquimbensis male to change sex observed in the different experimental treatments. Vertical lines on each bar correspond to 1 standard error. (B) Relationship between growth rate and time in days that the males spent on the female in the copulatory position in three social composition treatments where a female was present.

Figure 6

The average time (A) and body size (B) at which sex change occurred for C. coquimbensis males placed in differing social aggregations. Vertical lines on each bar correspond to 1 standard deviation.

Figure 7. Frequency of male individuals observed at different rankings of reproductive success and time to sex change in two experimental social aggregations, 1F+2M and 1F+4M, of C. coquimbensis.

Results are shown for estimations before and after intracapsular cannibalism. A ranking of 1 for reproductive success corresponds to the male with the highest value, meanwhile, a ranking of 1 for sex change corresponds to males that changed earliest.