Abstract
Background: In protandric-simultaneous (PS) hermaphrodites, individuals invariably reproduce as males first and later in life as simultaneous hermaphrodites. Here, the shrimp Lysmata wurdemanni was used as a model to (i) test for the role of sexual selection (male-male competition) in explaining the early male phase and size-dependent sex allocation (SDSA) in PS hermaphrodites, (ii) examine the tradeoff between the male and female function in hermaphrodites, and (iii) determine if SDSA also takes place in the form of sex-specific behaviors and anatomical structures. Results: In L. wurdemanni, male mating ability was size- and sex-dependent; greater for small than for large hermaphrodites and for males than hermaphrodites matched in body size. The above explains the adaptive value of the early male phase in PS hermaphrodites; small individuals should speed up sperm production and delay female reproduction to profit from male mating opportunities that are the greatest when small. Size-dependent male mating ability also suggests that small hermaphrodites should produce proportionally more sperm than ova compared to large hermaphrodites, a prediction supported by data. Sex allocation, measured as sex-specific behaviors and anatomical structures, was also size-dependent. No tradeoff between ova and sperm mass was found. However, among-individual variation in resource acquisition was considerable, suggesting that the observed lack of a statistical relationship between sperm and ova mass does not necessarily imply the absence of sex allocation tradeoffs in L. wurdemanni. Conclusion: Sexual selection is most relevant in PS hermaphrodites, SDSA also involves sex-specific behaviors and morphological features, and variation in resource acquisition and allocation can explain the apparent absence of sex allocation tradeoffs.
Highlights
Examples of mixed sexual systems include androdioecy [males coexist with hermaphrodites in a population: e.g., the conchostracan shrimp Eulimnadia texana (Zucker et al, 1997), the fish Kryptolebias marmoratus (Mackiewicz et al, 2006)], bidirectional sex change [individuals shift from one sex to the other more than once during lifetime: the fish Lythrypnus dalli (Mary, 1994) and Gobiodon histrio (Munday et al, 1998)] and size-dependent sex allocation (SDSA) in species initially classified as strict simultaneous hermaphrodites [investment to the sex functions shifts with body size in various fish and worms (Petersen and Fischer, 1996; Schärer et al, 2001; Vizoso and Schärer, 2007)]
In 8 out of 30 replicates, insemination occurred during the moment of molting, and in 7 out of these 8 replicates, the shrimp inseminating this “parturial” hermaphrodite was the small male
Small males were nearly twice more successful in inseminating parturial shrimps than were male-role hermaphrodites when insemination occurred during the moment of molting, no significant difference was observed between males and hermaphrodites in male mating ability (P = 0.3633)
Summary
The importance of sexual selection in shaping individual traits (e.g., anatomical, physiological, and behavioral) and population parameters (e.g., sex ratio, sexual dimorphism, migration, life history schedules) is well established in gonochoristic species (separate sexes) and, to a lesser extent, in strictly sequential and simultaneous hermaphrodites [separate sexes (Emlen and Oring, 1977; Andersson, 1994; Shuster and Wade, 2003), hermaphrodites (Warner et al, 1975; Arnqvist and Rowe, 2005; Koene, 2006; Leonard, 2006; Michiels and Koene, 2006; Munday et al, 2006; Petersen, 2006; West, 2009; Schärer and Pen, 2013)]. Protandric simultaneous hermaphroditism is suspected in other taxa [e.g., fish, snails, barnacles (Ghiselin, 1969, 1974; Fischer, 1981; Charnov, 1982, 1987; Policansky, 1982; Crisp, 1983; Michiels, 1998; Chaine and Angeloni, 2005)] In these sequential-simultaneous hermaphrodites, sexual selection might be relevant to explain (i) the adaptive value of the adolescent male phase and (ii) the optimal investment to the male and female function (i.e., sex allocation) during the hermaphroditic phase. Sequential-simultaneous hermaphrodites serve as model systems to (iii) test predictions at the core of life-history and sex allocation theories; i.e., trade-offs between the sex functions (Charnov, 1982, 1987; Stearns, 1992; Roff, 2002; West, 2009)
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