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Social Control of Reproduction and Breeding Monopolization in the Eusocial Snapping Shrimp Synalpheus Elizabethae W&M ScholarWorks VIMS Articles Virginia Institute of Marine Science 11-2015 Social Control of Reproduction and Breeding Monopolization in the Eusocial Snapping Shrimp Synalpheus elizabethae STC Chak Virginia Institute of Marine Science DR Rubenstein JE Duffy Virginia Institute of Marine Science Follow this and additional works at: https://scholarworks.wm.edu/vimsarticles Part of the Ecology and Evolutionary Biology Commons, and the Marine Biology Commons Recommended Citation Chak, STC; Rubenstein, DR; and Duffy, JE, Social Control of Reproduction and Breeding Monopolization in the Eusocial Snapping Shrimp Synalpheus elizabethae (2015). American Naturalist, 186(5), 660-668. 10.1086/683132 This Article is brought to you for free and open access by the Virginia Institute of Marine Science at W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. vol. 186, no. 5 the american naturalist november 2015 Natural History Note Social Control of Reproduction and Breeding Monopolization in the Eusocial Snapping Shrimp Synalpheus elizabethae Solomon T. C. Chak,1,* Dustin R. Rubenstein,2 and J. Emmett Duffy1,† 1. Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, Virginia 23062; 2. Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, New York 10027 Submitted February 17, 2015; Accepted June 4, 2015; Electronically published September 15, 2015 Online enhancements: appendixes. Dryad data: http://dx.doi.org/10.5061/dryad.6vb73. abstract: Understanding why individuals within altruistic socie- a continuum based on reproductive skew (Keller and Reeve ties forgo reproduction to raise others’ offspring has fascinated scien- 1994; Keller and Perrin 1995; Sherman et al. 1995), the tists since Darwin. Although worker polymorphism is thought to have monopolization of breeding positions appears to be main- evolved only in sterile workers, worker subcastes appear to be com- tained differently in different taxa (Crespi and Yanega 1995). mon among social invertebrates and vertebrates. We asked whether Worker sterility—adefining characteristic of caste differen- sterility accompanies eusociality and morphological differentiation in tiation in eusocial species (Crespi and Yanega 1995; Boom- — snapping shrimps (Synalpheus) the only known marine eusocial group. sma 2007, 2009)—occurs in a variety of obligatorily euso- We show that workers in Synalpheus elizabethae are reproductively to- tipotent and that female—but not male—gonadal development and mat- cial insects (e.g., several ant genera, corbiculate bees, vespine ing are mediated by the presence of a queen, apparently without phys- wasps, and higher termites; Wilson 1971; Fletcher and Ross ical aggression. In queenless experimental colonies, a single immature 1985; Thorne et al. 2003; Ratnieks et al. 2006), where work- female worker typically became ovigerous, and no female workers ma- ers are irreversibly committed to their nonreproductive roles tured in colonies with a resident queen. Thus, eusocial shrimp work- (Boomsma 2013). In contrast, helpers in all cooperatively ers retain reproductive totipotency despite signs of morphological spe- breeding vertebrates (birds and mammals), as well as work- cialization. The failure of most female workers to mature is instead ers in most facultatively eusocial insects (e.g., halictid bees, facultative and mediated by the presence of the queen, ensuring her re- productive monopoly. gall-forming thrips, and lower termites; Faulkes 1990; Chap- man et al. 2002; Hart and Ratnieks 2005; Hartke and Baer Keywords: eusociality, reproductive skew, reproductive conflict, re- 2011), are totipotent and retain the ability to reproduce. productive suppression, sterility, totipotency. Most facultatively eusocial species outside of the Hyme- noptera are fortress defenders (Queller and Strassmann 1998) that nest within rich, concentrated food sources (e.g., clonal Introduction gall-forming aphids, ambrosia beetles, wood-dwelling ter- Societies characterized by cooperation and reproductive al- mites, thrips, and two species of mole rats). However, very truism occur across the animal tree of life in a range of ver- few—if any—of these fortress defenders, other than the tebrate and invertebrate taxonomic groups (Wilson 1971; higher termites, have evolved obligatory eusociality with an Buskirk 1981; Brown 1987; Duffy 1996; Solomon and French irreversible worker caste (Abe 1987; Noirot and Pasteels 1997; Strassmann et al. 2000). Eusocial societies character- 1987). Why obligatory eusociality has evolved in higher ized by cooperative offspring care, overlapping generations, termites but not in other fortress defenders remains unclear and reproductive division of labor (castes; Michener 1969; but may be related to food resources. Unlike most other Wilson 1971) represent the pinnacle of social evolution but fortress defenders, termites are central place foragers that share many characteristics with other forms of altruistic obtain food from outside of the nest (Higashi et al. 1991; groups. Although social animals have been suggested to form Heinze and Korb 2008; Boomsma 2013). Additionally, long- lived host fortresses have been hypothesized to play a key role in the evolution of obligate eusociality (e.g., the am- * Corresponding author; e-mail: [email protected]. † brosia beetle Austroplatypus incompertus;KentandSimpson Present address: Tennenbaum Marine Observatories Network, Smithsonian Institution, P.O. Box 37012, NHB MRC 106, Washington, DC 20013. 1992; Boomsma 2013), though this idea has not been tested. Am. Nat. 2015. Vol. 186, pp. 660–668. q 2015 by The University of Chicago. The evolution of an irreversible worker caste is thought 0003-0147/2015/18605-56065$15.00. All rights reserved. to be an important precursor to the evolution of morpho- DOI: 10.1086/683132 logical polymorphism of workers in eusocial species (i.e., This content downloaded from 128.239.099.140 on May 05, 2019 14:59:31 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). Worker Totipotency in a Eusocial Shrimp 661 the presence of specialized worker subcastes), because it logical differentiation between queens and workers is sug- allows colony-level selection to enhance worker efficiency gestive of a true worker caste, similar to that observed in and reproductive fitness of the colony (Oster and Wilson the eusocial ambrosia beetle (Kent and Simpson 1992). Ad- 1979). In support of this hypothesis, sterile workers in ants ditionally, large colonies of eusocial Synalpheus in several and higher termites show the most extreme forms of worker species exhibit a morphologically specialized group of large morphological and ecological polymorphism (Wilson 1971). individuals that possess a bigger weapon (fighting claw) than Yet some fortress defenders express morphological differ- other workers and who are more active in colony defense entiation among nonreproductives that are reproductively but show no external signs of reproductive maturity (Duffy totipotent, including soldier neotenics in lower termites 1998; Duffy et al. 2002; Tóth and Duffy 2008). These shrimp (Thorne et al. 2003) and the dispersive morph in naked mole workers resemble the morphologically specialized caste in rats (O’Riain et al. 1996). Therefore, it has been hypothe- many obligatory eusocial insects, such as ants and higher sized that the presence of polymorphic reproductive sol- termites, or facultatively eusocial species, such as lower ter- diers may represent a natural transition toward obligate mites and naked mole rats, that have reproductively toti- eusociality (Thorne et al. 2003; Boomsma 2013). However, potent workers. it is not yet clear whether worker sterility is a necessary con- Here we explore whether the fortress defender S. eliza- dition for the evolution of irreversible worker castes (i.e., bethae shows parallels with other social insects and verte- obligatory eusociality), especially when observations have brates in how eusociality, worker sterility, and morpholog- been limited to only a few lineages of insects and a single ver- ical differentiation have coevolved. Our primary goal is tebrate group. to determine whether a eusocial species of Synalpheus has Exploring the generality of the relationship between either reproductively totipotent workers that might repre- worker sterility and worker polymorphism requires study- sent an early stage of social evolution or sterile workers that ing a range of animal lineages with a diversity of social sys- might facilitate evolution of worker polymorphism, as in the tems. An ideal study species would be a noninsect, eusocial Hymenoptera (Crespi and Yanega 1995; Boomsma 2013). fortress defender such as the snapping shrimp Synalpheus We first test whether workers in S. elizabethae have lost elizabethae. Synalpheus shrimps live obligatorily within ca- or maintained the ability to reproduce by examining go- nals of live marine demosponges, which are stable, predator- nadal development. We then report on experiments designed free, and typically long-lived fortresses (McMurray et al. 2008). to determine whether workers are capable of mating in the Like most other fortress defenders, Synalpheus shrimps do absence of the queen and whether mediation of worker de- not forage outside of the host sponge. Instead, they feed velopment involves aggression
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