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The Speciation History of Heliconius: Inferences from Multilocus DNA Sequence Data

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The Speciation History of Heliconius: Inferences from Multilocus DNA Sequence Data The speciation history of Heliconius: inferences from multilocus DNA sequence data by Margarita Sofia Beltrán A thesis submitted for the degree of Doctor of Philosophy of the University of London September 2004 Department of Biology University College London 1 Abstract Heliconius butterflies, which contain many intermediate stages between local varieties, geographic races, and sympatric species, provide an excellent biological model to study evolution at the species boundary. Heliconius butterflies are warningly coloured and mimetic, and it has been shown that these traits can act as a form of reproductive isolation. I present a species-level phylogeny for this group based on 3834bp of mtDNA (COI, COII, 16S) and nuclear loci (Ef1α, dpp, ap, wg). Using these data I test the geographic mode of speciation in Heliconius and whether mimicry could drive speciation. I found little evidence for allopatric speciation. There are frequent shifts in colour pattern within and between sister species which have a positive and significant correlation with species diversity; this suggests that speciation is facilitated by the evolution of novel mimetic patterns. My data is also consistent with the idea that two major innovations in Heliconius, adult pollen feeding and pupal-mating, each evolved only once. By comparing gene genealogies from mtDNA and introns from nuclear Tpi and Mpi genes, I investigate recent speciation in two sister species pairs, H. erato/H. himera and H. melpomene/H. cydno. There is highly significant discordance between genealogies of the three loci, which suggests recent speciation with ongoing gene flow. Finally, I explore the phylogenetic relationships between races of H. melpomene using an AFLP band tightly linked to the Yb colour pattern locus (which determines the yellow bar in the hindwing). At this locus, races group according to geographical location rather than clades inferred from colour pattern phenotype. This and similar loci can be used to facilitate comparative mapping with other Heliconius species. In summary, the patterns at each phylogenetic level using different gene regions are consistent with a scenario of rapid, adaptively driven divergence and speciation in this group. 2 Querido Eduardo, poeta de Colombia: Cuando por muchos años y por muchas regiones mi pensamiento se detenía en Colombia, se me aparecía tu vasta tierra verde y forestal, el río Cauca hinchado por las lágrimas de María y planeando sobre todas las tierras y los ríos, como pañuelos de terciopelo celestial, las extraordinarias mariposas amazónicas, las mariposas de Muzo. Siempre vi tu país al través de una luz azul de mariposas bajo este enjambre de alas ultravioleta, y vi también los caseríos desdoblados en este tembloroso vaivén de alas, y luego vi la historia de Colombia seguida por un cometa de mariposas azules: sus grandes capitanes, Santander, Bolívar con una mariposa luminosa posada en cada hombro, como la más deslumbrante charretera, y a tus poetas, infortunados como José Asunción o como Porfirio o soberbios como Valencia, perseguidos hasta el fin de su vida por una mariposa, que olvidaban de pronto en el sombrero o en un soneto, mariposa que voló cuando Silva consumó su romántico suicidio para posarse más tarde tal vez sobre tus sienes, Eduardo Carranza. Pablo Neruda poeta chileno en homenaje al poeta colombiano Eduardo Carranza (1946) Nada me apartará del corazón verde de Colombia... Mi poesía seguirá celebrándote, Esmeralda. Luego el Museo de Oro Precolombino: con sus máscaras, collares, caracoles, mariposas, ranitas refulgentes……. Pablo Neruda 3 Table of Contents Chapter 1 ......................................................................................................................................... 15 Do pollen feeding and pupal-mating have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data............................................................................................... 15 Abstract....................................................................................................................................... 15 Introduction................................................................................................................................ 15 Unique traits of Heliconius .................................................................................................... 15 Systematics in Heliconius butterflies..................................................................................... 18 Conflict between phylogenies................................................................................................ 23 Taxon sampling ................................................................................................................. 23 Number of informative characters .................................................................................... 23 Methods of tree reconstruction ......................................................................................... 24 Material and methods ............................................................................................................... 28 Sampling methods .................................................................................................................. 28 Molecular regions and sequencing methods.......................................................................... 28 Mitochondrial DNA .......................................................................................................... 28 Nuclear loci........................................................................................................................ 30 Alignment and phylogenetic analyses ................................................................................... 31 Results ......................................................................................................................................... 32 Characterisation of the nucleotide data.................................................................................. 32 Mitochondrial DNA .......................................................................................................... 33 Nuclear DNA..................................................................................................................... 33 Models of sequence evolution........................................................................................... 35 Congruence test ................................................................................................................. 36 Phylogenetic analyses............................................................................................................. 36 Discussion ................................................................................................................................... 43 Relationships in the melpomene/cydno and silvaniform group ............................................ 44 Pupal-mating clade................................................................................................................. 45 Paraphyletic taxa..................................................................................................................... 46 Conclusions................................................................................................................................. 48 References................................................................................................................................... 49 Chapter 2 ......................................................................................................................................... 54 Species diversity and speciation in Heliconius butterflies: inferences from species level phylogeny.......................................................................................................................................... 54 Abstract....................................................................................................................................... 54 Introduction................................................................................................................................ 54 Heliconius butterflies: a model to study speciation .............................................................. 56 4 Phylogenetic tests of speciation............................................................................................. 58 Methods....................................................................................................................................... 60 Phylogeny ............................................................................................................................... 60 Geographical isolation............................................................................................................ 62 Comparative analysis ............................................................................................................. 63 Results ......................................................................................................................................... 66 Geographical isolation............................................................................................................ 66 Comparative analysis ............................................................................................................. 68 Discussion ..................................................................................................................................
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