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Morphological Phylogeny of Alpheid Shrimps: Parallel Preadaptation and the Origin of a Key Morphological Innovation, the Snapping Claw

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Morphological Phylogeny of Alpheid Shrimps: Parallel Preadaptation and the Origin of a Key Morphological Innovation, the Snapping Claw Evolution, 60(12), 2006, pp. 2507-2528 MORPHOLOGICAL PHYLOGENY OF ALPHEID SHRIMPS: PARALLEL PREADAPTATION AND THE ORIGIN OF A KEY MORPHOLOGICAL INNOVATION, THE SNAPPING CLAW ARTHUR ANKER,12 SHANE T. AHYONG,34 PIERRE Y. NOEL,5-6 AND A. RICHARD PALMER1-7 l Systematics and Evolution Group, Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada ^Department of Marine Invertebrates, Australian Museum, 6 College Street, Sydney, New South Wales 2010, Australia 5Departement Milieux et Peuplements Aquatiques, Unite Scientifique Museum 0401, UMR CNRS-UPMC-MNHN BOME 8044, Biologie des Organismes Marins et Ecosystemes, Museum National d'Histoire Naturelle, 61 rue Buffon, 75005, Paris, France ^E-mail: [email protected] 7E-mail: rich.palmer®ualberta.ca Abstract.—The Alpheidae—possibly the most diverse family of recent decapod crustaceans—offers attractive oppor- tunities to study the evolution of many intriguing phenomena, including key morphological innovations like spectacular snapping claws, highly specialized body forms, facultative and obligate symbioses with many animal groups, and sophisticated behaviors like eusociality. However, studies of these remarkable adaptations remain hampered by in- sufficient phylogenetic information. We present the first phylogenetic hypothesis of relationships among 36 extant genera of alpheid shrimps, based on a cladistic analysis of 122 morphological characters from 56 species, and we use this hypothesis to explore evolutionary trends in morphology and species diversity. Our results strongly supported a monophyletic Alpheidae that included two hitherto difficult-to-place genera (Yagerocaris and Pterocaris). Of 35 + nodes among genera, all were supported by at least one morphological character (24 were supported by two or more) and 17 received greater than 50% jackknife support. Unfortunately, many basal nodes were only weakly supported. Six genera appeared nonmonophyletic, including the dominant genus Alpheus (paraphyletic due to inclusion of one clade with three minor genera). Evolutionary trends in alpheid claw form shed some revealing light on how key innovations evolve. First, several functionally significant features of the cheliped (claw bearing leg) evolved inde- pendently multiple times, including: asymmetry, folding, inverted orientation, sexual dimorphism, adhesive plaques that enhance claw cocking, and tooth-cavity systems on opposing claw fingers, a preadaptation for snapping. Many conspicuous features of alpheid claw form therefore appear prone to parallel evolution. Second, although tooth-cavity systems evolved multiple times, a functional snapping claw, which likely facilitated an explosive radiation of over 550 species, evolved only once (in Synalpheus + [Alpheus + satellite genera]). Third, adhesive plaques (claw cocking aids) also evolved multiple times, and within snapping alpheids are associated with the most diverse clade (Alpheus + derivative genera). This pattern of parallel preadaptation—multiple independent evolutionary origins of precursors (preadaptations) to what ultimately became a key innovation (adaptation)—suggests alpheid shrimp claws are pre- disposed to develop features like tooth-cavity and adhesive plaque systems for functional or developmental reasons. Such functional/developmental predisposition may facilitate the origin of key innovations. Finally, moderate orbital hoods—anterior projections of the carapace partly or completely covering the eyes—occur in many higher Alpheidae and likely evolved before snapping claws. They are unique among decapod crustaceans, and their elaboration in snapping alpheids suggests they may protect the eyes from the stress of explosive snaps. Thus one key innovation (orbital hoods) may have facilitated evolution of a second (snapping claws). Key words.—Alpheidae, adaptive radiation, character evolution, Crustacea, Decapoda, novelty, parallel evolution. Received August 30, 2005. Accepted August 2, 2006. Parallelism, Preadaptation, and Key Innovations typically reflects an adaptive response to similar conditions (Futuyma 1998). Such parallel adaptive responses may be Examples of parallel evolution—the independent origin of facilitated by similar genetic (Schluter et al. 2004) or de- functionally and structurally similar traits among closely re- velopmental (Nijhout 1991) avenues. Furthermore, phylo- lated tax a—occur in many groups of organisms (Futuyma inno i ->nm c ii i inni, c i n r genetic tests of adaptation (e.g., correlations between form 1998; Levin 2001; Schlutert ett al. 2004). Such parallelisms, , , . , ^ , ■ . , , ,, . , ,. ' . , , and function or between form and environment) and the evo- oft course, pose problems for cladistic analysis because char lution of development are greatly strengthened where mul- acter state codings are based on similarity; homology (or tiple independent contrasts (Felsenstein 1985) provided by homoplasy) can only be judged from tree topology after the parallel or convergent evolution are possible (Palmer 2004). analysis. However, parallel evolution can provide strong ev- Less well appreciated is how patterns of parallel evolution idence for adaptation: the independent origin of functionally may shed valuable light on the evolutionary origin of key and structurally similar traits in separate but related clades innovations. (We use the term "key innovation" in the sense of Mayr (1960): a functionally significant synapomorphy as- 2 Present address: Smithsonian Tropical Research Institute, Apar- sociated with and presumed to have facilitated a major adap- tado 0843-03092, Balboa, Ancon, Panama, Republics de Panama; tiye radiation.) Darwin, like many others since (e.g., Mayr ^ ^Pres^adS^Marine Biodiversity and Biosecurity, National ^O; Nitecki 1990; Muller and Wagner 1991), was troubled Institute of Water and Atmospheric Research, Private Bag 14901, by how novel forms arise: "Why . should there be so Kilbirnie, Wellington, New Zealand; E-mail: [email protected]. much variety and so little real novelty?" (Darwin 1872, 2507 © 2006 The Society for the Study of Evolution. All rights reserved. 2508 ARTHUR ANKER ET AL. p. 156). One recurring hurdle to our understanding of how other caridean shrimp (cf. Fig. 4n). Others are greatly en- key innovations arise evolutionarily is their rarity: often, they larged (Figs. lc,j-o,r-t; 3d,f-j; online Fig. S2a,b,f), often arise only once within a clade (Vermeij 2006) so the only highly asymmetrical (Figs. lj,n,s,t; 3d,f-j; online Figs. S2i, clues about origins lie in fossils or living descendents of taxa S3), and sometimes specialized and oddly shaped (see Fig. immediately ancestral to the clade defined by the key inno- 4p,t,v,x; online Fig. S3b). Cheliped polymorphism and sexual vation. Therefore, multiple independent origins of putative dimorphism occur in many genera (e.g., Banner and Banner precursor states—structurally or functionally intermediate 1982; Anker et al. 2001; Anker 2003b, see also online Fig. preadaptations—permit more rigorous tests of the ecological S3). correlates of key innovations. In the most diverse alpheid clade {Alpheus + Synalpheus Here we describe a pattern that offers promise for under- + derivative genera), one of the first pereiopods (chelipeds) standing the evolutionary origin of key innovations: parallel bears a voluminous claw with a complex snapping mecha- preadaptation. This term refers to the multiple independent nism on the fingers: the snapping claw (Fig. 5g-i). The snap- evolutionary origins of precursors (preadaptations) to what ping claw is a powerful, multifunctional tool used for defense ultimately became a key innovation (adaptation) with a whol- and aggression in interspecific and agonistic interactions ly new function in one or a few clades. We illustrate this (e.g., Hazlett and Winn 1962; Schultz et al. 1998; Schmitz phenomenon with a phylogenetic study of alpheid shrimps, and Herberholz 1998; Duffy et al. 2002). The loud snap, one a spectacularly diverse clade of caridean shrimps within of the most audible and familiar of underwater noises, is which an undeniable key innovation evolved: the snapping detectable as far away as one kilometer (M. Chitre, pers. claw. comm.). The crackling noise produced by numerous snapping shrimps may interfere with submarine sonar system, and it Alpheid Ecological Diversity prompted extensive investigations following World War II (Johnson et al. 1947) to the present day (e.g., Chitre 2005). The caridean shrimp family Alpheidae, which includes Most early workers who studied snapping in Alpheus and over 600 species in 36+ genera, is an abundant and ecolog- Synalpheus believed impact of the dactylus (movable finger) ically diverse group of decapod crustaceans. Most alpheids on the pollex (fixed finger) caused the snap (e.g., Coutiere inhabit marine, shallow tropical and subtropical waters (e.g., 1899; Volz 1938; Knowlton and Moulton 1963; Ritzmann Chace 1988), although some live in cool-temperate waters 1974). However, dramatic evidence from Alpheus hetero- (e.g., Anker and Jeng 2002; Anker and Komai 2004; Fig. li). chaelis (Versluis et al. 2000) revealed that the snap results A few have colonized oligohaline or freshwater habitats (e.g., from implosion of a cavitation bubble caused by water rapidly Powell 1979; Yeo and Ng 1996), whereas others are stygo- bitic or stygophilic (e.g., Hobbs 1973; Anker and Iliffe 2000). ejected from a socket in the fixed finger by a plunger (spe- Alpheids also live in mangroves and estuarine areas (e.g., cialized tooth)
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