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Parsing Parallel Evolution: Ecological Divergence and Differential Gene Expression in the Adaptive Radiations of Thick-Lipped Midas Cichlid fishes from Nicaragua

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Parsing Parallel Evolution: Ecological Divergence and Differential Gene Expression in the Adaptive Radiations of Thick-Lipped Midas Cichlid fishes from Nicaragua Molecular Ecology (2012) doi: 10.1111/mec.12034 Parsing parallel evolution: ecological divergence and differential gene expression in the adaptive radiations of thick-lipped Midas cichlid fishes from Nicaragua TEREZA MANOUSAKI,*†1 PINCELLI M. HULL,*‡1 HENRIK KUSCHE,*§ GONZALO MACHADO-SCHIAFFINO,* PAOLO FRANCHINI,* CHRIS HARROD,¶**†† KATHRYN R. ELMER*‡‡ and AXEL MEYER*†§ *Lehrstuhl fu¨r Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universita¨tsstrasse 10, 78457 Konstanz, Germany, †Konstanz Research School Chemical Biology (KoRS-CB), University of Konstanz, Universita¨tsstrasse 10, 78457 Konstanz, Germany, ‡Department of Geology and Geophysics, Yale University, PO Box 208109, New Haven, CT, 06520- 8109, USA, §International Max Planck Research School for Organismal Biology, University of Konstanz, Universita¨tsstrasse 10, 78457, Konstanz, Germany, ¶Department of Evolutionary Genetics, Max Planck Institute for Limnology, PO Box 165, 24302 Plo¨n, Germany, **School of Biological Sciences, Queen’s University, Belfast, 97 Lisburn Road, Belfast, BT9 7BL, UK, ††Instituto de Investigaciones Oceanolo´gicas, Universidad de Antofagasta, Avenida Angamos 601, Antofagasta, Chile Abstract The study of parallel evolution facilitates the discovery of common rules of diversifica- tion. Here, we examine the repeated evolution of thick lips in Midas cichlid fishes (the Amphilophus citrinellus species complex)—from two Great Lakes and two crater lakes in Nicaragua—to assess whether similar changes in ecology, phenotypic trophic traits and gene expression accompany parallel trait evolution. Using next-generation sequencing technology, we characterize transcriptome-wide differential gene expres- sion in the lips of wild-caught sympatric thick- and thin-lipped cichlids from all four instances of repeated thick-lip evolution. Six genes (apolipoprotein D, myelin-associ- ated glycoprotein precursor, four-and-a-half LIM domain protein 2, calpain-9, GTPase IMAP family member 8-like and one hypothetical protein) are significantly underex- pressed in the thick-lipped morph across all four lakes. However, other aspects of lips’ gene expression in sympatric morphs differ in a lake-specific pattern, including the magnitude of differentially expressed genes (97-510). Generally, fewer genes are differ- entially expressed among morphs in the younger crater lakes than in those from the older Great Lakes. Body shape, lower pharyngeal jaw size and shape, and stable isotopes (d13C and d15N) differ between all sympatric morphs, with the greatest differ- entiation in the Great Lake Nicaragua. Some ecological traits evolve in parallel (those related to foraging ecology; e.g. lip size, body and head shape) but others, somewhat surprisingly, do not (those related to diet and food processing; e.g. jaw size and shape, stable isotopes). Taken together, this case of parallelism among thick- and thin-lipped cichlids shows a mosaic pattern of parallel and nonparallel evolution. Keywords: crater lakes, divergent selection, geometric morphometrics, next-generation sequencing, RNA-Seq, sympatric speciation Received 30 March 2012; revision received 11 June 2012; accepted 26 July 2012 Correspondence: Axel Meyer, Fax: +49 7531 883018; Introduction E-mail: [email protected] ‘Parallel phenotypic evolution’ describes the repeated, ‡‡ Present address: College of Medical, Veterinary & Life Sciences, Institute of Biodiversity, Animal Health & Compara- independent evolution of similar phenotypes in tive Medicine, University of Glasgow, Glasgow, UK. closely related lineages (reviewed in Elmer & Meyer 1Co-first authors. 2011). Many classic cases of ecological speciation are, © 2012 Blackwell Publishing Ltd 2 T. MANOUSAKI ET AL. in fact, examples of parallel evolution (Schluter 2000; marine populations in generating repeated, similar Salzburger & Meyer 2004), including the Holarctic mar- phenotypes (Schluter & Conte 2009). How, when and to ine to freshwater invasions of stickleback fishes (Bell & what extent parallel phenotypes evolve under a nonpar- Foster 1994), adaptive radiations such as Darwin’s allel genetic basis may prove as interesting as the paral- finches on the Galapagos Islands (Grant & Grant 2008) or lel examples, because it suggests restricted phenotypic cichlid fishes in African and Central American lakes solutions to ecological problems (Losos 2011; Wake et al. (Meyer 1993; Barlow 2000). Instances of parallel evolution 2011). raise the question, how and why does evolution repeat Recent advances in DNA sequencing technology itself in similar environments? Specifically, we can ask: allow the rapid acquisition of vast, genomic-scale does the repeated evolution of a similar trait coincide resources and permit the collection of transcriptomic with parallel ecological and transcriptomic diversifica- data for ecological as well as evolutionary model tion, or are similar phenotypes evolving by different eco- species (Stapley et al. 2010). Before sequence-based logical and genomic mechanisms? Recent advances on transcriptomics, it was microarrays and qPCR tech- this fundamental topic in evolutionary biology (Meyer niques based on a priori sequence information that 1999; West-Eberhard 2002; Sanetra et al. 2005; Losos 2011) revealed the importance of gene expression differentia- have been aided by comparative developmental analyses tion in the diversification of natural populations and new genomic approaches –including the (Oleksiak et al. 2002; Storey et al. 2007; Pavey et al. transcriptome-wide expression analyses as we use here 2010), particularly in the phenotypic divergence of tele- (Johnson et al. 2010; Mahler et al. 2010; Kolbe et al. 2011; ost populations (e.g. Derome et al. 2006; Kobayashi et al. Kusumi et al. 2011; Losos & Pringle 2011; Eckalbar et al. 2006; St-Cyr et al. 2008). Comparative transcriptomic 2012; Sanger et al. 2012). approaches permit an expanded purview into gene Differences in gene expression or gene sequence can expression by detecting differential expression in novel directly underpin ecologically relevant phenotypic genes and the interaction of many genes of small effect variation in populations (e.g. Oleksiak et al. 2002; (Mackay et al. 2009; Stapley et al. 2010), both of which Whitehead & Crawford 2006; Hoekstra & Coyne 2007), are likely to be important in the evolution of novel phe- thus providing the raw material upon which selection notypes. In short, both the novel genomic tools—and acts (Ellegren & Sheldon 2008). Gene expression and the morphological and ecological tools—now exist to function link the genotype to the phenotype and, in this parse evolutionary events into their repeated vs. unique role, are central to understanding adaptation, pheno- components in cases of repeated evolution of particular typic diversification, repeated evolution and ecological phenotypic traits (e.g. Manceau et al. 2010; Elmer & speciation (e.g. Sanetra et al. 2005; Manceau et al. 2010; Meyer 2011). Here, we leverage these new tools to Pavey et al. 2010). For instance, in Darwin’s finches and investigate the similarity of ecomorphological and tran- African cichlids, it is variation in the expression of bmp4 scriptomic changes accompanying the repeated evolu- that is linked to phenotypic variation in beak and jaw tion of hypertrophied lips in Central American Midas morphology, ecologically relevant morphological traits cichlid fishes (Amphilophus species complex, Gunther essential for each groups’ adaptive radiation (Abzhanov 1864) from the Great Lakes and crater lakes of Nicara- et al. 2004; Albertson et al. 2005). In three-spined gua (Fig. 1). sticklebacks, pelvic reduction repeatedly evolved via a Midas cichlids provide repeated natural experiments reduction of Pitx1 expression, with fixation in popula- in ecological speciation (Barlow & Munsey 1976; Meyer tions dependent on factors such as the presence of 1990a; Elmer et al. 2010a). In Nicaragua, tectonic and gape-limited predators and calcium limitation, among volcanic activity led to the formation of numerous, others (Shapiro et al. 2004; Chan et al. 2010). small crater lakes. At least eight crater lakes were colo- However, parallel phenotypic evolution does not nized by Midas cichlids originating from the Great always arise from parallel genomic and transcriptomic Lakes–Lake (L.) Managua and L. Nicaragua (Wilson changes (reviewed in Elmer & Meyer 2011). At the et al. 2000; Barluenga & Meyer 2004, 2010; Elmer et al. genomic level, either standing genetic variation or new 2010b, 2012). In several isolated crater lakes, similar mutations can be the target of selection (reviewed in morphological types are repeatedly observed, including Barrett & Schluter 2008). For example, the parallel evo- a deep-body benthic morph, an elongate, limnetic lution of cryptic coat coloration in Peromyscus mice is morph and a thick-lipped morph (reviewed in Elmer driven by an assortment of changes in gene function et al. 2010a). Despite the similarity of these repeated and expression, and the fixation of ancestral or, at phenotypes, phylogenetic analyses have shown that times, unique, derived genetic mutations (reviewed in individuals within any given crater lake are more Manceau et al. 2010). In freshwater sticklebacks, selec- closely related to one another than they are to individu- tion repeatedly favours alleles present in the ancestral als in any other lake (Wilson et al. 2000; Barluenga & © 2012 Blackwell Publishing Ltd REPEATED EVOLUTION OF THICK LIPS IN MIDAS CICHLIDS 3 L. Nicaragua L. Apoyeque Managua
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