Genetic Divergence Among Sympatric Colour Morphs of the Dalmatian Wall Lizard (Podarcis Melisellensis)
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Genetica (2010) 138:387–393 DOI 10.1007/s10709-010-9435-2 Genetic divergence among sympatric colour morphs of the Dalmatian wall lizard (Podarcis melisellensis) K. Huyghe • M. Small • B. Vanhooydonck • A. Herrel • Z. Tadic´ • R. Van Damme • T. Backeljau Received: 10 September 2009 / Accepted: 5 January 2010 / Published online: 19 January 2010 Ó Springer Science+Business Media B.V. 2010 Abstract If alternative phenotypes in polymorphic pop- genetic divergence, indicating that gene flow is somewhat ulations do not mate randomly, they can be used as model restricted among morphs and suggesting possible adaptive systems to study adaptive diversification and possibly the diversification. early stages of sympatric speciation. In this case, non random mating is expected to support genetic divergence Keywords Polymorphism Á FST Á FIS Á among the different phenotypes. In the present study, we Non-random mating Á Population divergence Á use population genetic analyses to test putatively neutral Microsatellites genetic divergence (of microsatellite loci) among three colour morphs of the lizard Podarcis melisellensis, which is associated with differences in male morphology, per- Introduction formance and behaviour. We found weak evidence of Phenotypic polymorphisms are a prominent form of diver- sification in many animal taxa, and a fascinating aspect of K. Huyghe (&) Á B. Vanhooydonck Á R. Van Damme Á T. Backeljau biological diversity. They are often used as model systems Department of Biology, University of Antwerp, in studies central to evolutionary biology. The long term Universiteitsplein 1, 2610 Antwerp, Belgium maintenance of alternative morphs in a population implies e-mail: [email protected] that all morphs have equivalent fitnesses, and often the M. Small different morphs show differences in other phenotypic traits Molecular Genetics Laboratory, Washington Department of Fish as well. When alternative morphs coexist in a population, and Wildlife, 600 Capitol Way N, Olympia, WA 98502, USA correlational (or epistatic) selection may favor certain trait combinations at the expense of other combinations, which A. Herrel De´partement d’Ecologie et de Gestion de la Biodiversite´, may result in modifications of the genetic architecture and C.N.R.S/M.N.H.N, 57 rue Cuvier, Case postale 55, 75231 Paris developmental pathways and lead to genetic divergence Cedex 5, France among morphs (Lande and Arnold 1983; Forsman and Appelqvist 1998; Forsman et al. 2008). In resource based or Z. Tadic´ Department of Animal Physiology, University of Zagreb, trophic polymorphisms for example, discrete morphs can Rooseveltov trg 6, Zagreb 10000, Croatia show differential morphological adaptations and resource use (see review in Smith and Sku´lason 1996). In other cases, T. Backeljau phenotypic polymorphisms have been linked to alternative Royal Belgian Institute of Natural Sciences, Vautierstraat 29, 1000 Brussels, Belgium reproductive strategies (Oliveira et al. 2008), with accom- panying differences in size, shape, and/or performance Present Address: (Sinervo et al. 2000; Meyers et al. 2006; Pryke and Griffith K. Huyghe 2006; Huyghe et al. 2007). Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales (MNCN-CSIC), Calle Jose´ Phenotypic morphs associated with alternative repro- Gutie´rrez Abascal 2, 28006 Madrid, Spain ductive strategies are usually found to be adaptive 123 388 Genetica (2010) 138:387–393 (Brockmann and Taborsky 2008). Polymorphisms may be occur in three different phenotypes (morphs): they show the outcome of phenotypic plasticity (condition-depen- white, yellow or orange ventral coloration (Huyghe et al. dence), may be highly genetically determined, or may be 2007). Male morphs show differences in size, head shape, the result of a combination of the two. Further differenti- jaw muscle mass, bite force capacity and fighting ability ation could then be promoted in the presence of non-ran- (Huyghe et al. 2007, 2009a), while female morphs do not dom mating barriers such as positive assortative mating differ in any of the aforementioned traits (Huyghe et al. among individuals of the same morphotype or selection unpublished data). We therefore assume that these male against hybrids. This could theoretically lead to reproduc- morphs have evolved as alternative ‘‘tactics’’ to deal with tive isolation between morphotypes, even in the absence of different selective pressures partly shaped by sexual temporal or spatial segregation. Genetic divergence selection, while the mechanisms through which female between such sympatric morphs provides an outstanding morphs originated remain unknown. The relative frequen- opportunity to study the early stages of adaptive diversifi- cies of the morphs within a population of P. melisellensis cation and sympatric speciation (Smith and Sku´lason 1996; and individual coloration seem to remain stable across Hendry et al. 2009). years (Huyghe et al. unpublished data). Polymorphisms in Whether and how often sympatric speciation occurs in coloration or colour patterns are widespread in natural natural populations are much debated topics, but different populations, and have contributed significantly to the speciation models have demonstrated the theoretical fea- understanding of the conditions that promote the evolution sibility and some empirical examples are available. Theo- and maintenance of polymorphisms (Sinervo et al. 2007; retical models have been described for sympatric Forsman et al. 2008; Svensson et al. 2009). As the colour speciation through natural and sexual selection (Lande and morphs in P. melisellensis are associated with morph-spe- Kirkpatrick 1986; Van Doorn and Weissing 2001; Gavrilet cific suites of characters, positive assortative mating might and Waxman 2002;Ha¨rdling and Bergsten 2006), but these promote increased phenotypic and genetic divergence, and models also have identified many possible constraints on eventually complete reproductive isolation. Hence, this diversification in sympatry (Coyne and Orr 2004; Bolnick polymorphic population provides an ideal study system to and Fitzpatrick 2007). Empirical evidence of reproductive test genetic divergence by non-random (assortative) isolation and incipient sympatric speciation through natural mating. selection (ecological speciation) has been found in several The random mating hypothesis for permanent poly- studies. For instance, in the marine periwinkle (Littorina morphism states that different morphs of a polymorphic saxatilis), males prefer females of their own ecotype (Jo- population can successfully interbreed so that random hannessen et al. 2008), and in Darwin’s finches (Geospiza mating occurs (Ford 1945). In this context, we tested the fortis) there is strong assortative pairing within small and null hypothesis of random mating, i.e. lack of genetic large beak morphs, resulting in restricted gene flow divergence, among colour morphs in the polymorphic liz- between these morphs (Huber et al. 2007). Other examples ard Podarcis melisellensis. of sympatric speciation have been found in stickleback fish (McKinnon and Rundle 2002), Rhagoletis flies (Linn et al. 2004), and other herbivorous insects (e.g. Funk et al. 2002; Methods Matsubayashi et al. 2009). Sexual selection as a sole mechanism driving sympatric speciation is unlikely in the Field methods absence of any ecological diversification (Coyne and Orr 2004; Van Doorn et al. 2004; Bolnick and Fitzpatrick 2007; Podarcis melisellensis is a medium-sized lacertid lizard Ritchie 2007), but sexual selection could be responsible for occurring along the Adriatic coast and on islands in the mating polymorphisms, possible cradles for additional Adriatic Sea. Populations of P. melisellensis seem to vary (ecological) sources of disruptive selection. in their degree of polymorphism; some populations To test genetic divergence among alternative sympatric (islands) include one, two, or three colour (Huyghe et al. morphs, one must identify genetically diverged subpopu- pers. obs.). On the island of Lastovo (Croatia, 42°160N, lations (morphs) and assign individuals (probabilistically) 16°540E, 53 km2), lizards have a bright white, yellow or to these subpopulations. The highest resolution to estimate orange ventral colour. These three morphs are distributed relatedness among individuals of unknown pedigree can be randomly and share the same microhabitat (Huyghe et al. achieved by using data from highly polymorphic loci. In 2007). During fieldtrips in 2006 and 2007, we collected a this study we estimated the putatively neutral divergence at small piece of tail tissue (\3 mm) from 271 individuals of microsatellite loci between colour morphs of a population this population, comprising 140 males (78 white, 32 yellow of the lizard Podarcis melisellensis, occurring on the island and 30 orange) and 131 females (98 white, 25 yellow and 8 of Lastovo, Croatia. In this population, males and females orange). Tail tissue was preserved in 95% ethanol for 123 Genetica (2010) 138:387–393 389 transport and storage until DNA analysis (Huyghe et al. alleles, stuttering and/or differential amplification effi- 2009b). ciency of large vs small alleles (large allele dropout). We tested for linkage disequilibrium between pairs of loci using Laboratory processing Genepop v.3.3. across and within colour morph classes. Genetic heterogeneity among colour morphs was ana- Microsatellite genotypes from 13 loci were used to assess lysed in several ways. First, we tested for differences in gene flow and genetic