9 · The expression of crustacean mating strategies STEPHEN M. SHUSTER CHAPTER SUMMARY strategies are represented and opportunities for further research abound. Three fundamental patterns of phenotypic expression exist Several frameworks for understanding alternative mat- for alternative mating strategies. These patterns include ing strategies now exist (Gadgil 1972, Maynard Smith 1982, Mendelian strategies, developmental strategies, and Austad 1984, Dominey 1984, Gross 1985, 1996, Lucas and behavioral strategies. Each pattern of expression is revealed Howard 1995, Gross and Repka 1998). Because these by hormonal and neurological factors that regulate the approaches have focused primarily on behavioral or deve- timing and degree to which phenotypic differences appear; lopmental differences among individuals (that is, on however, the nature of each regulatory mechanism depends “condition-dependent phenotypes” often called “tactics” fundamentally on its underlying mode of inheritance. The (Box 9.1), and because such polymorphisms seldom conform genetic architectures underlying such inheritance in turn to the simplifying assumptions required by game theory depend on the circumstances in which mating opportunities regarding inheritance and fitness, there has been little con- arise, including the intensity of selection favoring distinct sensus about the theoretical and empirical approaches best reproductive morphologies, and the predictability of mating suited for investigating alternative mating strategies and opportunities within individual lifespans. This chapter tactics, in the laboratory as well as in nature. concerns the nature of this variation and its possible causes, In response to this confusion, Shuster and Wade (2003; with illustrations from the Crustacea. see also Hazel et al. 1990, Roff 1992, 1996, Sinervo 2000, 2001, Shuster 2002) explained how alternative mating strat- 9.1 INTRODUCTION egies can be understood using conventional evolutionary Although crustaceans were among the first recorded genetic principles including game theory, provided that the examples of alternative mating strategies (Orchestia darwinii: average as well as the variance in fitness among the observed Darwin 1874, p. 275; Tanais spp.: Darwin 1874, p. 262), morphs is considered within quantitative analyses. This there is currently no synthetic treatment of how such requirement is necessary because alternative mating strat- polymorphisms are expressed within this group. The egies evolve in response to sexual selection, an evolutionary apparent scarcity of reports of male polymorphism among context in which fitness variance is often extreme. When crustaceans is unexpected given the frequency with which fundamental principles are applied, the contexts in which sexual selection has been demonstrated within this taxon alternative mating strategies evolve as well as the forms these (Holdich 1968, 1971, Manning 1975, Stein 1976, Thompson adaptations assume become clear. and Manning 1981, Knowlton 1980, Shuster 1981, This chapter has three parts. First, I will explain the Christy 1983, Hatziolos and Caldwell 1983, reviews in source of sexual selection and how it produces alternative Salmon 1984, Koga et al. 1993). As explained below, when mating strategies in the first place. Second, I will describe sexual selection occurs, alternative mating strategies are Levins’ (1968) scheme for understanding polyphenism (the likely to evolve. This chapter provides an evolutionary tendency for individuals to express variable phenotypes in framework for understanding the expression of alternative response to environmental cues) to show why alternative mating strategies, with illustrations from the Crustacea mating strategies can be understood in this light (see (Table 9.1). My goals are to show that in this fascinating Shuster and Wade 2003). Third, using crustacean collection of species, all known forms of alternative mating examples, I will demonstrate how this approach predicts the Alternative Reproductive Tactics, ed. Rui F. Oliveira, Michael Taborsky, and H. Jane Brockmann. Published by Cambridge University Press. ª Cambridge University Press 2008. 224 Table 9.1. A preliminary taxonomic distribution of alternative mating strategies within the Crustacea Taxon Species Conventional morph Alternative morph(s) Mode of expression References Branchiopoda Anostraca Eubranchipus serratus Guard individual females in Usurper Behavioral Belk 1991 sequence Notostraca Triops newberryi Hermaphrodite Male Mendelian Sassaman 1991 Conchostraca Eulinmadia texana Hermaphrodite Male Mendelian Sassaman 1989, Sassaman and Weeks 1993, Weeks and Zucker 1999 Maxillipoda Copepoda Euteropina acutifrons Large males Small males Mendelian/develop- Haq 1965, 1972, 1973, mental D’Apolito and Stancyk 1979, Moreira et al. 1983, Moreira and McNamara 1984, Stancyk and Moreira 225 1988 Malacostraca Stomatopoda Pseudosquilla ciliata Guard individual females in Usurper Behavioral Hatziolos and sequence Caldwell 1983 Gonodactylus bredini Guard individual females in Usurper Behavioral Shuster and Caldwell sequence 1989 Decapoda Caridea Alpheus armatus Guard individual or groups of Usurper/sneaker? Behavioral Knowlton 1980 females Argis dentata Protandrous hermaphrodites Primary females Developmental? Fre´chette et al. 1970 Athanas spp. Protandrous hermaphrodites Primary males Developmental? Nakashima 1987, Gherardi and Calloni 1993 Crangon crangon Protandrous hermaphrodites Primary females Developmental? Boddeke et al. 1991 Exhippolysmata sp. Protandrous simultaneous Developmental? Bauer 2002 hermaphrodites Lysmata spp. Protandrous simultaneous Developmental Bauer 2000, Baeza and hermaphrodites Bauer 2004 Macrobrachium dayanum Guard female groups Female mimic, sneaker Developmental Kuris et al. 1987 Table 9.1 (cont.) Taxon Species Conventional morph Alternative morph(s) Mode of expression References Macrobrachium idea Guard female groups Female mimic, sneaker Developmental Kuris et al. 1987 Macrobrachium malcolmsonii Guard female groups Female mimic, sneaker Developmental Kuris et al. 1987 Macrobrachium rosenbergii Guard female groups Female mimic, sneaker Developmental Nagamine et al. 1980, Ra’anan and Sagi 1989, Kuris et al. 1987, Barki et al. 1992, Karplus et al. 2000, Kurup et al. 2000 Macrobrachium rosenbergii Large females Small females Unknown Harikrishnan et al. 1999 Macrobrachium scabriculum Guard female groups Female mimic, sneaker Developmental Kuris et al. 1987 Pandalus spp. Protandrous hermaphrodites Primary females Developmental? Charnov 1979, 1982, Bergstro¨m 1997 Processa edulis Protandrous hermaphrodites Primary females Developmental? Noe¨l 1976 Rhynchocinetes typus Guard individual females in Sneaker (intermedius), Behavioral Correa et al. 2000, 226 sequence (robustus, sperm competitor 2003, Correa and intermedius) (typus) Thiel 2003 Thor manningi Protandrous hermaphrodites Primary males Developmental? Chace 1972, Bauer 1986 Brachyura Callinectes sapidus Guard individual females in Usurper Behavioral/develop- Jivoff and Hines 1998 sequence mental Chionoecetes opilio Smooth spermatophores Wrinkled spermato- Unknown Moriyasu and phores Benhalima 1998 Inachus phalangium Mate with many females in Sperm competitors Behavioral Diesel 1989 sequence Libinia emarginata Guard individual females in Usurper (small males) Developmental Sagi et al. 1994, Ahl sequence (large males) and Laufer 1996 Pachygrapsus transversus Guard female groups (large Sneaker (small males) Behavioral/develop- Abele et al. 1986 males) mental Scopimera globosa Guard resources required by Usurpers/wanderers Behavioral/develop- Wada 1986, Koga 1998 females (males occupy (small males) mental burrows) Uca spp. Guard resources required by Usurpers/wanderers Behavioral Salmon and Hyatt females (males occupy 1983, Christy and burrows) Salmon 1991, Jennions and Backwell 1998 Palinura Jasus edwardsii Mate with many females in Sperm competitor Behavioral MacDiarmid and sequence Butler 1999 Dendrobrachiata Sicyonia dorsalis Mate with many females in Sperm competitor? Behavioral Bauer 1992 sequence Astacidea Homarus americanus Guard individual females in Usurper Behavioral Cowan and Atema sequence 1990, Cowan 1991 Amphipoda Jassa falcata Guard individual females in Sneaker (thumbless Developmental Borowsky 1985 sequence (thumbed males) males) Jassa marmorata Guard individual females in Sneaker (thumbless Developmental Clark 1997, Kurdziel sequence (thumbed males) males) and Knowles 2002 Microdeutopus gryllotalpa Guard individual females in Sneaker (thumbless Developmental Borowsky 1980, 1984, sequence (thumbed males) males) 1989 Orchestia darwinii Guard individual females in Sneaker (thumbless Developmental? Darwin 1874 sequence (thumbed males) males) Isopoda Elaphognathia cornigera Guard female groups (large Sneaker (small males) Unknown Tanaka and Aoki 1999, 227 males) Tanaka 2003 Idotea baltica Guard individual females in Usurper Behavioral Jormalainen et al. 1994 sequence Jaera albifrons Guard individual females in Unknown, males with Mendelian Bocquet and Veuille sequence (males with setose nonsetose walking legs 1973 walking legs) Paracerceis sculpta Guard female groups (a- Female mimic (b- Mendelian Shuster 1989, 1992, males) males), sneaker (c- Shuster and Wade males) 1991, 2003, Shuster and Sassaman 1997, Shuster and Levy 1999, Shuster et al. 2001 Thermosphaeroma spp. Guard individual females in Usurper Behavioral Shuster 1981, sequence Jormalainen and Shuster 1999 Tanadiacea Tanais spp. Guard individual females in Sneaker