Habitat Partitioning and Morphological Differentiation: the Southeast Asian Draco Lizards and Caribbean Anolis Lizards Compared
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Oecologia (2014) 175:651–666 DOI 10.1007/s00442-014-2921-y COMMUNITY ECOLOGY - ORIGINAL RESEARCH Habitat partitioning and morphological differentiation: the Southeast Asian Draco lizards and Caribbean Anolis lizards compared Terry J. Ord · Danielle A. Klomp Received: 21 July 2013 / Accepted: 5 March 2014 / Published online: 22 March 2014 © Springer-Verlag Berlin Heidelberg 2014 Abstract Sympatric species that initially overlap in perch use in the same way as it was in Anolis: species that resource use are expected to partition the environment in used wider perches exhibited longer limb lengths. These ways that will minimize interspecific competition.T his results provide an important illustration of how interspe- shift in resource use can in turn prompt evolutionary cific competition can occur along common ecological axes changes in morphology. A classic example of habitat parti- in different animal groups, and how natural selection along tioning and morphological differentiation are the Caribbean these axes can generate the same type of adaptive change in Anolis lizards. Less well studied, but nevertheless strik- morphology. ing analogues to the Anolis are the Southeast Asian Draco lizards. Draco and Anolis have evolved independently of Keywords Adaptation · Convergence · Ecobehavior · each other for at least 80 million years. Their compari- Ecomorphology · Limb length son subsequently offers a special opportunity to examine mechanisms of phenotypic differentiation between two ecologically diverse, but phylogenetically distinct groups. Introduction We tested whether Draco shared ecological axes of dif- ferentiation with Anolis (e.g., habitat use), whether this When taxa that exploit similar ecological resources come differentiation reflected interspecific competition, and to into contact, the ensuing competition between these taxa what extent adaptive change in morphology has occurred can exert considerable selection pressure for one or both to along these ecological axes. Using existing data on Ano- diverge in habitat use to minimize ecological competition. lis, we compared the habitat use and morphology of Draco This shift can lead to phenotypic differentiation among taxa in a field study of allopatric and sympatric species on the in ecologically relevant characters as each taxon becomes Malay Peninsula, Borneo and in the Philippines. Sympatric adapted to its change in habitat use, a phenomenon known Draco lizards partitioned the environment along common as character displacement (Brown and Wilson 1956). Char- resource axes to the Anolis lizards, especially in perch use. acter displacement from interspecific competition has been Furthermore, the morphology of Draco was correlated with viewed as an important engine of evolutionary diversifi- cation (Dayan and Simberloff 2005; Pfennig and Pfennig 2012; Stuart and Losos 2013). A classic example is the Communicated by Lin Schwarzkopf. adaptive radiation of the Caribbean Anolis lizards. Sym- patric Anolis species have diverged in perch use and other Electronic supplementary material The online version of this resources to minimize ecological overlap and subsequent article (doi:10.1007/s00442-014-2921-y) contains supplementary material, which is available to authorized users. competition (e.g., Losos 1990b, 1992; see also Stuart and Losos 2013). This is believed to have promoted the evolu- T. J. Ord (*) · D. A. Klomp tion of up to six different microhabitat specialists distinct in Evolution and Ecology Research Centre, and the School morphology and behavior, termed “ecomorphs” (Williams of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, NSW 2052, Australia 1983). The Anolis are an especially powerful illustration e-mail: [email protected] of how ecological competition can drive morphological 1 3 652 Oecologia (2014) 175:651–666 differentiation because of the level of replication exhibited that occupy a range of comparable and diverse tropical within the group: the same set of Anolis microhabitat eco- habitats (Schwartz and Henderson 1991; Grismer 2011), morphs have independently evolved repeatedly on each of have social systems centered on males defending territories the four Greater Antillean islands (Losos et al. 1998). (Hairston 1957; Ord 2008), and communicate using elabo- Shared adaptive responses to common selection pres- rate visual displays that are remarkable in their similarity sures in congeners are understandable given that closely (Mori and Hikida 1994; Ord and Martins 2006). Third, related species share much of their genome. That is, the both genera are species rich; Caribbean Anolis especially adaptive convergence of the Anolis ecomorphs on each so with over 150 species (Losos 2009), while Draco is island has presumably been facilitated by the fact that all of more moderately diverse with at least 45 species (McGuire the lizards of this genus have inherited part of their genome and Dudley 2011). Finally, species in both genera are often from the same evolutionary ancestor, which has predis- found at high densities with several congeners at the same posed these lizards to adapt in similar ways (e.g., Wood location (Inger 1983; Schwartz and Henderson 1991), et al. 2005). The extent to which more distantly related spe- implying interspecific competition is potentially important cies (e.g., from different families) follow the same evolu- for Draco in the same way it has been for the Anolis lizards tionary trajectories when exposed to similar forms of selec- (Losos 1994). tion is less clear. Increasing phylogenetic distance between We conducted our comparison of the evolutionary dif- taxa tends to accentuate the signature of stochasticity in ferentiation of the Anolis and Draco lizards in three parts. evolutionary differentiation through processes such as First, we compared the level of functionally relevant mor- genetic drift and random mutation (Lenormand et al. 2009). phological differentiation among Draco species with The history of past adaptations and different functional comparison to the Anolis adaptive radiation. Second, we trade-offs or genetic correlations between aspects of the assessed whether morphological variation among Draco phenotype can also mean taxa from diverse phylogenetic species exhibited patterns of adaptive evolution similar to backgrounds respond very differently to common selection the Anolis lizards. Finally, we examined the extent to which pressures (e.g., Alfaro et al. 2005; Ord et al. 2011). In light Draco species have shifted resource use in the presence of of these variables, any similarity in the outcome of adaptive ecologically similar congeners, and whether this occurs evolution between highly divergent, phylogenetic groups along the same axes as the Anolis lizards. would reveal the extent that natural selection can override In Anolis, interspecific competition has prompted micro- stochastic processes and historical contingencies to repeat- habitat differentiation along several ecological axes, but edly produce similar phenotypes. predominately perch size and perch height (e.g., Schoener With this in mind, we examined whether similarities 1968; Pacala and Roughgarden 1982; Rummel and Rough- in habitat use—and subsequent similarities in selection— garden 1985; Losos et al. 1993). Shifts in perch use have between two highly divergent lineages of lizard have pro- in turn resulted in adaptive differentiation in morphology, duced the same adaptive changes in morphology, and particularly limb length (Losos et al. 1997, 2004) and, at whether interspecific competition along the same ecologi- its ultimate conclusion, this differentiation probably culmi- cal axes has potentially played a role in diversification in nated in the evolution of the ecomorphs (Losos 2009). Spe- both groups. These lineages were the Southeast Asian cific adaptations in limb length to perch use result because Draco lizards and the Greater Antillean Anolis lizards. As lizards with shorter limbs are more agile on smaller, irregu- alluded to above, the adaptive radiation of the Anolis liz- lar-shaped perches, whereas lizards with longer limbs have ards and the relationship between interspecific competition, higher running speeds and better jumping capabilities on habitat use and morphological evolution have been exten- wider, more even surfaces (e.g., Losos and Sinervo 1989; sively studied (reviewed by Losos 2009). We used these Irschick and Losos 1999; Toro et al. 2004). Limb length existing data on the Anolis lizards to benchmark a field has often evolved in concert with tail length (Losos 1990a) study of the habitat use and morphology of the Draco liz- and longer tails function to improve stability while jump- ards. This comparison of Draco and Anolis was pertinent ing between perches (Higham et al. 2001; Kuo et al. 2012). for several key reasons. First, the two genera are the prod- Other axes of ecological divergence among sympatric Ano- uct of distinct evolutionary histories. Each genus is nested lis include thermal microhabitat [e.g., perches in the sun within separate, ecologically diverse families—the Agami- vs. those in shade (see Williams 1983)] and diet [prey size dae and Iguanidae, respectively—that have not shared an (e.g., Schoener 1968; Pacala and Roughgarden 1985)]. evolutionary ancestor for 80-146 million years (Townsend To determine whether interspecific competition among et al. 2011; Daza et al. 2012; Mulcahy et al. 2012; Pyron Draco might have also occurred along these same ecologi- and Burbrink 2014).