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Limited Evidence for Unusual Body Size Evolution on Islands

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Limited Evidence for Unusual Body Size Evolution on Islands Journal of Biogeography (J. Biogeogr.) (2011) 38, 89–100 ORIGINAL Slaying dragons: limited evidence for ARTICLE unusual body size evolution on islands Shai Meiri1*, Pasquale Raia2 and Albert B. Phillimore3 1Department of Zoology, Faculty of Life ABSTRACT Sciences, Tel Aviv University, 69978 Tel Aviv, Aim Island taxa often attain forms outside the range achieved by mainland Israel, 2Dipartimento di Scienze della Terra, Universita` Federico II, 80138 Naples, Italy, relatives. Body size evolution of vertebrates on islands has therefore received 3Division of Biology, Imperial College at much attention, with two seemingly conflicting patterns thought to prevail: (1) Silwood Park, Ascot SL5 7PY, UK islands harbour animals of extreme size, and (2) islands promote evolution towards medium body size (‘the island rule’). We test both hypotheses using body size distributions of mammal, lizard and bird species. Location World-wide. Methods We assembled body size and insularity datasets for the world’s lizards, birds and mammals. We compared the frequencies with which the largest or smallest member of a group is insular with the frequencies expected if insularity is randomly assigned within groups. We tested whether size extremes on islands considered across mammalian phylogeny depart from a null expectation under a Brownian motion model. We tested the island rule by comparing insular and mainland members of (1) a taxonomic level and (2) mammalian sister species, to determine if large insular animals tend to evolve smaller body sizes while small ones evolve larger sizes. Results The smallest species in a taxon (order, family or genus) are insular no more often than would be expected by chance in all groups. The largest species within lizard families and bird genera (but no other taxonomic levels) are insular more often than expected. The incidence of extreme sizes in insular mammals never departs from the null, except among extant genera, where gigantism is marginally less common than expected under a Brownian motion null. Mammals follow the island rule at the genus level and when comparing sister species and clades. This appears to be driven mainly by insular dwarfing in large-bodied lineages. A similar pattern in birds is apparent for species within orders. However, lizards follow the converse pattern. Main conclusions The popular misconception that islands have more than their fair share of size extremes may stem from a greater tendency to notice gigantism and dwarfism when they occur on islands. There is compelling evidence for insular dwarfing in large mammals, but not in other taxa, and little evidence for the second component of the island rule – gigantism in small-bodied taxa. *Correspondence: Shai Meiri, Department of Keywords Zoology, Faculty of Life Sciences, Tel Aviv University, 69978 Tel Aviv, Israel. Birds, dwarfism, evolution, gigantism, island biogeography, island rule, lizards, E-mail: [email protected] mammals. pygmy humans all spring to mind when the body sizes of INTRODUCTION island vertebrates is discussed. Body size evolution on islands is Giant tortoises, enormous flightless birds and huge bears, perceived to be fast (Lister, 1989; Millien, 2006) and has alongside minute deer, tiny lizards, dwarf elephants and, lately, produced extreme phenotypes, with the smallest or the largest ª 2010 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi 89 doi:10.1111/j.1365-2699.2010.02390.x S. Meiri et al. species of many clades being insular (Hooijer, 1967; Berry, mixed support for this rule (Clegg & Owens, 2002; Boback & 1998; Greer, 2001; Glaw et al., 2006; Whittaker & Ferna´ndez- Guyer, 2003; Lomolino, 2005; Meiri, 2007), with the best Palacios, 2007; Hedges, 2008; Losos & Ricklefs, 2009). For support coming from data for mammals (Lomolino, 1985; example, the St Helena earwig, Labidura herculeana, the Price & Phillimore, 2007; Welch, 2009; but see Meiri et al., Indonesian stick insect, Pharnacia serratipes, and the New 2004, 2006, 2008). Size evolution is often hypothesized to be Zealand giant wetas (Deinacrida spp.) are probably the largest most drastic on small islands, with island area showing representatives of their clades (Chown & Gaston, 2010). complex interactions with body size (Heaney, 1978), but Similarly, the world’s largest bat (Smith et al., 2003) is the empirical patterns are equivocal (e.g. Meiri et al., 2005b; Wu Philippine-endemic golden crowned flying fox, Acerodon et al., 2006; Schillaci et al., 2009). jubatus, the largest Quaternary bird was the Madagascan These two hypotheses, that islands should harbour extreme elephant bird, Aepyornis maximus, and the largest raptor was sizes, and that they should harbour taxa that are closer to a clade- the New Zealand endemic Haast’s eagle, Harpagornis moorei wide mode, need not necessarily be contradictory (Fig. 1). If a (Worthy et al., 2002; Murray & Vickers-Rich, 2004). clade, such as mammals, has a single size attractor (e.g. Brown Among reptiles, the largest living lizard (the Komodo et al., 1993) then members of a subclade may evolve to a size dragon, Varanus komodoensis) and tortoises (the giant tor- extreme: insular members of a subclade of large-bodied animals toises of Aldabra and the Galapagos, Geochelone gigantea and (e.g. elephants) will be the smallest within this subclade, but not Geochelone elephantopus) are insular endemics (Arnold, 1979; across the larger clade as a whole. Similarly, insular members of a Meiri, 2008). Islands also harbour the smallest members of subclade of small-bodied animals (e.g. shrews) may be the largest several clades: the smallest bird is believed to be the Cuban bee members of this subclade, but not the largest mammals overall. hummingbird, Mellisuga helenaei (although Dunning, 2008b, If, however, each subclade has its own optimal size that its insular suggests that Thaumastura cora from mainland Peru is members evolve towards (Lomolino, 2005) then islands should smaller), and species of Caribbean Leptotyphlops and Sphaero- harbour few size extremes (Fig. 1c). dactylus are the world’s smallest snakes and lizards, respectively The seemingly conflicting discussion of insular size extremes (Hedges, 2008; Meiri, 2008). This perceived abundance of on the one hand, and insular medium sizes on the other hand, insular size extremes is usually thought to be a response to the stems in part from the different phylogenetic and temporal scope low intensity of competition and predation both within and of studies dealing with them. Studies of size extremes are usually across taxa: the absence of carnivorous mammals is most often conducted at the inter-specific level (Glaw et al., 2006; Hedges, quoted as allowing the evolution of large size in birds (mainly 2008), and often deal with extinct taxa (Kurten, 1953; Sondaar, through the evolution of flightlessness; e.g. Bunce et al., 2005; 1977; Steadman et al., 2002; Raia et al., 2003). The study of Murray & Vickers-Rich, 2004), reptiles (e.g. Case, 1978; Meiri, evolution towards medium sizes usually involves intra-specific 2008) and small mammals (e.g. Angerbjo¨rn, 1986; Adler & studies of insular and mainland populations of extant species Levins, 1994). Alternatively, this perceived pattern may simply (e.g. Lomolino, 1985; Boback & Guyer, 2003; Meiri, 2007). reflect an ascertainment bias, i.e. we may be more likely to Evolutionary processes above and below the species level notice animals of extreme body size when they happen to live may differ through, for example, species sorting and adaptive on islands (Whittaker & Ferna´ndez-Palacios, 2007). radiation in the former versus inter-island and island– By contrast, the island rule suggests that, rather than showing mainland gene flow in the latter (Jablonski, 2008). As far as size extremes on islands, insular populations should be closer to we are aware McClain et al. (2006) and Welch (2010) present the clade-wide median body size than their mainland counter- the only purely inter-specific studies of the island rule, parts (Lomolino, 1985, 2005). According to the island rule, comparing mean sizes within genera of deep sea (= ‘insular’ populations of small species will evolve larger size, populations in McClain et al.) and shallow sea (‘mainland’) species, rather of large species will dwarf, and populations of average-sized than using comparisons within single species. An argument for species will show little size evolution on islands (Lomolino, 2005; extending tests of the island rule to the species level is that the Welch, 2009). Viewed at the clade level, the island rule predicts selection pressures thought to promote convergence on a stabilizing selection: on islands an individual should not be median body size for island populations should act similarly either too large or too small. Once the optimum is reached (via on island species. The major difference between the two directional selection on the founding population), stabilizing scenarios is that there should be less gene flow between species selection should maintain phenotypes around it. Interestingly, than between populations, meaning that evolution should an opposite pattern of disruptive selection and increased vari- proceed more rapidly in the former. However, there is no ance is often thought to prevail within populations on islands obvious reason why the type of selection and adaptive optima (Van Valen, 1965; Scott et al., 2003; cf. Meiri et al., 2005a). should differ in these two contexts. A major advantage of The island rule is thought to manifest the combined effects intra-specific
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