A Narrow Contact Zone Between Morphologically Cryptic Phylogeographic Lineages of the Rainforest Skink, Carlia Rubrigularis

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A Narrow Contact Zone Between Morphologically Cryptic Phylogeographic Lineages of the Rainforest Skink, Carlia Rubrigularis Evolution, 58(7), 2004, pp. 1536±1548 WHEN VICARS MEET: A NARROW CONTACT ZONE BETWEEN MORPHOLOGICALLY CRYPTIC PHYLOGEOGRAPHIC LINEAGES OF THE RAINFOREST SKINK, CARLIA RUBRIGULARIS BEN L. PHILLIPS,1 STUART J. E. BAIRD,2 AND CRAIG MORITZ3 Department of Zoology and Entomology, The University of Queensland, St Lucia, Queensland, 4067 Australia Abstract. Phylogeographic analyses of the fauna of the Australian wet tropics rainforest have provided strong evidence for long-term isolation of populations among allopatric refugia, yet typically there is no corresponding divergence in morphology. This system provides an opportunity to examine the consequences of geographic isolation, independent of morphological divergence, and thus to assess the broader signi®cance of historical subdivisions revealed through mitochondrial DNA phylogeography. We have located and characterized a zone of secondary contact between two long isolated (mtDNA divergence . 15%) lineages of the skink Carlia rubrigularis using one mitochondrial and eight nuclear (two intron, six microsatellite) markers. This revealed a remarkably narrow (width , 3 km) hybrid zone with substantial linkage disequilibrium and strong de®cits of heterozygotes at two of three nuclear loci with diagnostic alleles. Cline centers were coincident across loci. Using a novel form of likelihood analysis, we were unable to distinguish between sigmoidal and stepped cline shapes except at one nuclear locus for which the latter was inferred. Given estimated dispersal rates of 90±133 m 3 gen21/2 and assuming equilibrium, the observed cline widths suggest effective selection against heterozygotes of at least 22±49% and possibly as high as 70%. These observations reveal substantial postmating isolation, although the absence of consistent deviations from Hardy-Weinberg equilibrium at diagnostic loci suggests that there is little accompanying premating isolation. The tight geographic correspondence between transitions in mtDNA and those for nuclear genes and corresponding evidence for selection against hybrids indicates that these morphologically cryptic phylogroups could be considered as incipient species. Nonetheless, we caution against the use of mtDNA phylogeography as a sole criterion for de®ning species boundaries. Key words. Carlia rubrigularis, hybrid zone, likelihood pro®les, phylogeography, secondary contact, speciation. Received August 23, 2002. Accepted March 29, 2004. There is a general debate among evolutionary biologists lying patterns of genetic divergence (Ballard et al. 2002; about the nature of genetic differences that result in repro- Irwin 2002; Hudson and Turelli 2003). ductive isolation and the relative roles of isolation, genetic Analysis of zones of secondary contact between lineages drift, and divergent selection in speciation (e.g., Orr and can shed light on the extent and nature of reproductive iso- Smith 1998; Turelli et al. 2001; Gavrilets 2003). It is widely lation (Barton and Hewitt 1985, 1989). The majority of con- accepted that allopatric isolation combined with divergent tact zones concern taxa that are distinct phenotypically or selection on ecological or sexually dimorphic traits can result chromosomally and in many cases there is evidence for sub- in speciation, and it has also long been proposed that inci- stantial pre- and postzygotic isolation (Barton and Hewitt dental genetic divergence in allopatry can result in substantial 1985; Harrison 1993). However, despite the recent promi- postzygotic isolation (Dobzhansky 1937). Evidence for the nence given to phylogeographic structure as a criterion for latter comes in particular from experimental crosses of al- species recognition (e.g., Goldstein and DeSalle 2000; Tem- lopatric and morphologically cryptic sibling species (e.g., pleton 2001; Wiens and Penkrot 2002; Sites and Marshall Dobzhansky 1970). The recent emphasis on mtDNA phylo- 2003) and in conservation biology (Avise 2000; Moritz geography has revealed numerous cases of apparently deep 2002), there are remarkably few detailed studies of secondary historical subdivisions within species, many of which were contacts between lineages that are strongly differentiated in morphologically cryptic or even discordant with subspecies terms of mtDNA phylogeography, but which are morpho- boundaries (Avise 2000). However, it remains unclear wheth- logically cryptic (Hewitt 2001). er divergent mtDNA phylogroups represent organismal lin- The ``Wet Tropics'' rainforests of northeastern Australia eages that are independently evolving and perhaps intrinsi- offer an excellent natural laboratory for such studies. Com- cally isolated, or ones that will simply merge on secondary plementary biogeographic, palynological, and phylogeo- contact (Avise and Walker 1998; Wake and Schneider 1998). graphic data indicate that under cool-dry conditions that were Further, it is possible that, for one reason or another, mtDNA typical for much of the Quaternary, rainforest in this region phylogroups misrepresent organismal history and/or under- existed as two major isolates, each consisting of several smaller refugia (Webb and Tracey 1981; Nix 1991; Kershaw 1 Present address: Department of Biological Sciences, University 1994; Schneider et al. 1998; Hugall et al. 2002). The same of Sydney, New South Wales, 2006 Australia; E-mail: phillips@ bio.usyd.edu.au. evidence supports a rapid expansion of the rainforest during 2 Present address: Centre de Biologie et de Gestion des Popu- a cool-wet phase commencing approximately 8000 years ago lations, INRA-CBGP, Campus International de Baillarguet, CS 30 (Kershaw 1986; Walker 1990; Hopkins et al. 1993). Although 016 34988, Montferrier/Lez cedex, France; E-mail: stuart@ these data suggest long periods of isolation, it is also likely holyrood.ed.ac.uk. 3 Present address: Museum of Vertebrate Zoology, 3101 Life Sci- that populations restricted to these rainforest isolates have ences Building, University of California, Berkeley, California been subject to intermittent secondary contact during brief 94720-3160; E-mail: [email protected]. intervals when conditions were optimal for expansion of the 1536 q 2004 The Society for the Study of Evolution. All rights reserved. SECONDARY CONTACT IN CARLIA RUBRIGULARIS 1537 cool upland rainforests that harbor most of the endemic, rain- 2000). In the initial stages of any contact a cline in character forest-restricted species. This history of habitat contraction state frequencies must exist. The shape of the cline is deter- is re¯ected by a repeated pattern of strong mtDNA phylo- mined by the degree of selection against hybrids, the scale geographic structure between the two major isolates (Joseph of dispersal, and the time since contact (Endler 1977; Arnold et al. 1995; Schneider et al. 1998; Schneider and Moritz 1999; 1994). Neutral mixing and relatively large dispersal distances Hugall et al. 2002) with levels of intraspeci®c sequence di- will quickly result in a wide shallow cline whereas strong vergence sometimes approaching interspeci®c levels for the selection against hybrids, coupled with relatively small dis- taxa concerned (Moritz et al. 1997; Stuart-Fox et al. 2002). persal distances, will result in short, steep clines between Nevertheless, in all cases so far examined the highly diver- populations. A strong barrier to gene ¯ow between lineages gent phylogeographic lineages are morphologically cryptic would elicit the following characteristics: (1) substantial de- or separable only in multivariate space. (Schneider and Mo- viations from Hardy-Weinberg equilibrium at diagnostic loci ritz 1999; Schneider et al. 1999; M. Cunningham, unpubl. due to assortative mating and/or selection against hybrids; data). (2) a positive statistical association between loci for alleles These observations raise the question of whether the highly characteristic of each lineage (linkage disequilibrium) due to divergent phylogeographic lineages display any reproductive the dispersal of parental types into the zone and/or, the se- isolation, either pre- or postmating, or whether they simply lective removal of recombinant genotypes; and (3) clines that will merge when they come into contact. To address this remain narrow rather than widening under neutral diffusion. question, we analyzed a zone of secondary contact between Here we survey populations between the known locations divergent mtDNA phylogeogroups of the rainforest skink of the northern and southern lineages of C. rubrigularis to Carlia rubrigularis. These common, small (,52 mm snout/ locate a zone of secondary contact. We then characterize the vent), red-throated, and heliothermic skinks are endemic to zone using multiple molecular markers and analyze the data the Wet Tropics region (Nix and Switzer 1991; Cogger 2000). for patterns of genetic disequilibria and cline shape and The species is distributed across a wide variety of wet forest width. As cline width scales with dispersal, we also estimate habitats, typically at altitudes of less than 900 meters, and per generation dispersal distances from disequilibria within is most abundant in light gaps and along rainforest margins. the zone, and independently from isolation-by-distance Populations from the northern and southern wet tropics are among populations removed from the contact zone. reciprocally monophyletic for mtDNA with .15% net se- quence divergenceÐsimilar to that seen between recognized METHODS species of Carlia (Stuart-Fox et al. 2002). Multivariate anal- ysis of ®ve ecologically relevant morphological
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