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Sexual Selection and Mixed Sex Expression Clemson University TigerPrints Publications Biological Sciences 8-2018 Sexual Selection and Mixed Sex Expression: Adolescent Protandry, Phenotypic Tradeoffs and ‘Unconventional' Sex Allocation Estimates in a Protandric-Simultaneous Hermaphrodite J. Antonio Baeza Clemson University, [email protected] Follow this and additional works at: https://tigerprints.clemson.edu/bio_pubs Part of the Biology Commons Recommended Citation Baeza JA (2018) Sexual Selection and Mixed Sex Expression: Adolescent Protandry, Phenotypic Tradeoffs and ‘Unconventional' Sex Allocation Estimates in a Protandric-Simultaneous Hermaphrodite. Front. Mar. Sci. 5:260. doi: 10.3389/fmars.2018.00260 This Article is brought to you for free and open access by the Biological Sciences at TigerPrints. It has been accepted for inclusion in Publications by an authorized administrator of TigerPrints. For more information, please contact [email protected]. ORIGINAL RESEARCH published: 28 August 2018 doi: 10.3389/fmars.2018.00260 Sexual Selection and Mixed Sex Expression: Adolescent Protandry, Phenotypic Tradeoffs and ‘Unconventional’ Sex Allocation Estimates in a Protandric- Simultaneous Hermaphrodite J. Antonio Baeza 1,2,3* 1 Department of Biological Sciences, Clemson University, Clemson, SC, United States, 2 Smithsonian Marine Station at Fort Edited by: Pierce, Fort Pierce, FL, United States, 3 Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad XueWei Xu, Católica del Norte, Coquimbo, Chile Second Institute of Oceanography, State Oceanic Administration, China In protandric-simultaneous (PS) hermaphrodites, individuals invariably reproduce as Reviewed by: Mariano González-Castro, males first and later in life as simultaneous hermaphrodites. In this study, the shrimp Consejo Nacional de Investigaciones Lysmata wurdemanni (Gibbes, 1850) was used as a model to (i) test for the role of sexual Científicas y Técnicas (CONICET), Argentina selection (male-male competition) in explaining the early male phase and size-dependent Andrew Anthony David, sex allocation (SDSA) in PS hermaphrodites, (ii) examine the tradeoff between the male Clarkson University, United States and female function in hermaphrodites, and (iii) determine if SDSA also takes place in the *Correspondence: form of sex-specific behaviors and anatomical structures. In L. wurdemanni, male mating J. Antonio Baeza [email protected] 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 Specialty section: value of the early male phase in PS hermaphrodites; small individuals should speed up This article was submitted to Marine Evolutionary Biology, sperm production and delay female reproduction to profit from male mating opportunities Biogeography and Species Diversity, that are the greatest when small. Size-dependent male mating ability also suggests that a section of the journal Frontiers in Marine Science small hermaphrodites should produce proportionally more sperm than ova compared to large hermaphrodites, a prediction supported by data. Sex allocation, measured Received: 24 April 2018 Accepted: 13 July 2018 as sex-specific behaviors and anatomical structures, was also size-dependent. No Published: 28 August 2018 tradeoff between ova and sperm mass was found. However, among-individual variation in Citation: resource acquisition was considerable, suggesting that the observed lack of a statistical Baeza JA (2018) Sexual Selection and Mixed Sex Expression: Adolescent relationship between sperm and ova mass does not necessarily imply the absence Protandry, Phenotypic Tradeoffs and of sex allocation tradeoffs in L. wurdemanni. Sexual selection is most relevant in PS ‘Unconventional’ Sex Allocation hermaphrodites, SDSA also involves sex-specific behaviors, and morphological features, Estimates in a Protandric-Simultaneous and variation in resource acquisition and allocation can explain the apparent absence of Hermaphrodite. sex allocation tradeoffs. Front. Mar. Sci. 5:260. doi: 10.3389/fmars.2018.00260 Keywords: sexual selection, sex allocation, hermaphrodite, shrimp, crustacea Frontiers in Marine Science | www.frontiersin.org 1 August 2018 | Volume 5 | Article 260 Baeza Sexual-Selection & Sex-Allocation in Shrimp INTRODUCTION the sex functions (Charnov, 1982, 1987; Stearns, 1992; Roff, 2002; West, 2009). The importance of sexual selection in shaping individual traits (e.g., anatomical, physiological, and behavioral) and population The Adaptive Value of the Early Male Phase parameters (e.g., sex ratio, sexual dimorphism, migration, life in Protandric-Simultaneous history schedules) is well established in gonochoristic species (separate sexes) and, to a lesser extent, in strictly sequential Hermaphrodites and simultaneous hermaphrodites [separate sexes (Emlen and One hypothesis accounting for the adaptive value of the early Oring, 1977; Andersson, 1994; Shuster and Wade, 2003), male phase in protandric-simultaneous hermaphroditism, here hermaphrodites (Warner et al., 1975; Arnqvist and Rowe, 2005; named the “size-and-sex male advantage” hypothesis, argues Koene, 2006; Leonard, 2006; Michiels and Koene, 2006; Munday that male mating ability is sex- and size-dependent (Bauer, et al., 2006; Petersen, 2006; West, 2009; Schärer and Pen, 2013)]. 2002; Baeza, 2006, 2007a). If small individuals that allocate In contrast, sexual selection and its evolutionary consequences energy exclusively to male function are more successful in remain ill-explored in organisms with mixed sexual systems [for inseminating female-role hermaphrodites than other small exceptions see (Lorenzi et al., 2006; Weeks et al., 2006, 2014; individuals allocating energy to both ova and sperm, then Baeza, 2007a; Lorenzi and Sella, 2008; Benvenuto and Weeks, it is advantageous for hermaphrodites to invest more into 2012)]. male reproduction when small and to channel resources to In animals, examples of mixed sexual systems include the female function later in life, when their male mating androdioecy [males coexist with hermaphrodites in a population: ability has decreased substantially (Bauer, 2002; Baeza, 2007a). e.g., the conchostracan shrimp Eulimnadia texana (Zucker et al., This hypothesis also posits that it does not pay (in terms 1997), the fish Kryptolebias marmoratus (Mackiewicz et al., of fitness) for individuals to turn from functional males into 2006)], bidirectional sex change [individuals shift from one sex pure females when older and larger (as in strict sequential to the other more than once during lifetime: the fish Lythrypnus hermaphrodites) due to infrequent but reliable male mating dalli (Mary, 1994) and Gobiodon histrio (Munday et al., 1998)] opportunities later in life. Such rare but consistent male mating and size-dependent sex allocation (SDSA) in species initially opportunities imply male fitness gains favoring allocation to the classified as strict simultaneous hermaphrodites [investment to male function, to some extent, in larger, and older individuals the sex functions shifts with body size in various fish and worms (Baeza, 2007a). Previous studies testing for the adaptive value of (Petersen and Fischer, 1996; Schärer et al., 2001; Vizoso and protandric simultaneous hermaphroditism have focused on the Schärer, 2007)]. Species with peculiar sex expression patterns importance of sex-dependent time commitments, sex-dependent provide a useful model to test predictions fundamental to sexual energetic costs, and size-dependent mortality rates (Baeza, 2006). selection and sex allocation theories and to probe for the As yet, sexual selection has not been formally considered universality of sexual selection processes and consequences in as a mechanism accounting for the adaptive significance of animals. protandric simultaneous hermaphroditism. A rare mixed sexual system that may have arisen from sexual selection processes is protandric-simultaneous hermaphroditism Sex Allocation During the Simultaneous [called “adolescent protandry” sensu (Ghiselin, 1974) and Hermaphroditic Phase “protandric cosexuality” sensu (Policansky, 1982)]. In these In protandric simultaneous hermaphrodites, sexual selection species, individuals consistently mature and reproduce initially might have another important role in driving allocation to the as males and later in life, after attaining female function, male and female function during their terminal simultaneously turn to functional simultaneous hermaphrodites. Protandric hermaphroditic phase. Sexual selection (e.g., sperm competition) simultaneous hermaphroditism has been experimentally has been recognized as most relevant in shaping investment to confirmed in a polychaete worm (Premoli and Sella, 1995), sperm and ova in strict simultaneous hermaphrodites (Trouvé a land snail (Tomiyama, 1996), a tunicate (Manriquez and et al., 1999; Locher and Baur, 2000; Schärer and Ladurner, Castilla, 2005), a symbiotic barnacle (Crisp, 1983) and marine 2003; Tan et al., 2004; Schärer, 2009; Janicke et al., 2013, shrimps belonging to the genera Lysmata, Exhippolysmata, 2016). Theory predicts that simultaneous hermaphrodites should and Parhippolyte (Baeza, 2009, 2013; Braga et al., 2009; Baeza allocate proportionally more to male function when small et al., 2016a). Protandric simultaneous hermaphroditism is also than when large if their male mating ability is greater than suspected in other taxa [e.g., fish, snails, barnacles (Ghiselin, that of large conspecifics (Baeza, 2007a). Size-dependent
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