Luana Maroja | Williams College (original) (raw)

Papers by Luana Maroja

Insect Systematics & Evolution, Nov 1, 2017

Fireflies in the genus Photinus are well regarded for their luminescent nocturnal courtship displ... more Fireflies in the genus Photinus are well regarded for their luminescent nocturnal courtship displays. Here we report on a new firefly species, Photinus interdius, which is remarkable for its fully diurnal and luminescent courtship protocol. Males slowly flew near the ground searching for receptive females and emitted 800 ms, bright yellow light flashes at 3-4-s intervals. Male flights occurred as early as 13:10 and ceased before 18:00. We sequenced two mitochondrial loci and one genomic locus and combined these with those from 99 specimens representing 45 Photinus and 25 related firefly species. Bayesian inference resulted in a well-resolved phylogeny that placed this new species as the closest relative of, but basal to the Photinus clade. We propose that the adaptive significance of this extraordinary temporal shift in courtship niche is the outcome of a selective landscape that has optimized the trade-off between reduced predation risk and ease of mate-localization.

G3: Genes, Genomes, Genetics, Mar 1, 2016

The Heliconius butterflies are a widely studied adaptive radiation of 46 species spread across Ce... more The Heliconius butterflies are a widely studied adaptive radiation of 46 species spread across Central and South America, several of which are known to hybridize in the wild. Here, we present a substantially improved assembly of the Heliconius melpomene genome, developed using novel methods that should be applicable to improving other genome assemblies produced using short read sequencing. First, we wholegenome-sequenced a pedigree to produce a linkage map incorporating 99% of the genome. Second, we incorporated haplotype scaffolds extensively to produce a more complete haploid version of the draft genome. Third, we incorporated 20x coverage of Pacific Biosciences sequencing, and scaffolded the haploid genome using an assembly of this long-read sequence. These improvements result in a genome of 795 scaffolds, 275 Mb in length, with an N50 length of 2.1 Mb, an N50 number of 34, and with 99% of the genome placed, and 84% anchored on chromosomes. We use the new genome assembly to confirm that the Heliconius genome underwent 10 chromosome fusions since the split with its sister genus Eueides, over a period of about 6 million yr. KEYWORDS Heliconius genome assembly linkage mapping chromosome fusions Eueides Understanding evolution and speciation requires an understanding of genome architecture. Phenotypic variation within a population can be maintained by chromosome inversions (Lowry and Willis 2010; Joron et al. 2011; Wang et al. 2013), and may lead to species divergence (Noor et al. 2001; Feder and Nosil 2009) or to the spread of phenotypes by introgression (Kirkpatrick and Barrett 2015). Genetic divergence and genome composition is affected by variation in recombination rate (Nachman and Payseur 2012; Nam and Ellegren 2012). Gene flow between species can be extensive (Martin et al. 2013), and varies considerably across chromosomes (Via and West 2008; Weetman et al. 2012). Describing chromosome inversions, recombination rate variation, and gene flow in full requires as close to chromosomal assemblies of the genomes of study species as possible. Recombination rate varies along chromosomes and is influenced by chromosome length (Fledel-Alon et al. 2009; Kawakami et al. 2014), and inversions are often hundreds of kilobases to megabases long. However, many draft genomes generated with short-read technologies contain thousands of scaffolds, often

A major challenge in evolutionary biology is to understand the origins of novel structures. The w... more A major challenge in evolutionary biology is to understand the origins of novel structures. The wing patterns of butterflies and moths are derived phenotypes unique to the Lepidoptera. Here we identify a gene that we name poikilomousa (poik), which regulates colour pattern switches in the mimetic Heliconius butterflies. Strong associations between phenotypic variation and DNA sequence variation are seen in three different Heliconius species, in addition to associations between gene expression and colour pattern. Colour pattern variants are also associated with differences in splicing of poik transcripts. poik is a member of the conserved fizzy family of cell cycle regulators. It belongs to a faster evolving subfamily, the closest functionally characterised orthologue being the cortex gene in Drosophila, a female germ-line specific protein involved in meiosis. poik appears to have adopted a novel function in the Lepidoptera and become a major target for natural selection acting on colour and pattern variation in this group.

Understanding how speciation influences patterns of molecular evolution and how molecular changes... more Understanding how speciation influences patterns of molecular evolution and how molecular changes drive speciation are central questions in evolutionary biology. In this dissertation I address questions of behavioral barriers to gene exchange, cytoplasmic incompatibility, molecular evolution, population history, gene flow and species boundaries in the hybridizing field crickets Gryllus firmus and G. pennsylvanicus. I examine the role of behavioral barriers to gene exchange in the context of previous studies that documented temporal and ecological isolation and a one-way post-mating incompatibility. My results reveal strong behavioral premating barriers, but no apparent fecundity or fertility costs for G. firmus females when they mate with conspecific and heterospecific males. I also document a failure of heterospecific males to induce normal oviposition in G. firmus females, a previously unknown post-mating, pre-zygotic barrier. Gryllus firmus and G. pennsylvanicus exhibit a very clear unidirectional incompatibility and have been cited as a possible example of Wolbachia-induced cytoplasmic incompatibility. Wolbachia are cytoplasmically inherited alpha-proteobacteria that can cause cytoplasmic incompatibility in insects. I conduct curing experiments, intra-and interspecific crosses, cytological examination of Wolbachia in testes, and Wolbachia quantifications via Real-Time PCR. All of the data strongly suggest that Wolbachia are not involved in the reproductive incompatibility between G. firmus and G. pennsylvanicus. Finally I analyze DNA sequence divergence for seminal protein loci, housekeeping loci, and mtDNA, using a combination of analytical approaches and extensive sampling. In recently diverged species, such as G. firmus and G. pennsylvanicus, ancestral polymorphism and introgression can cause incongruence between gene trees and species trees. In the face of hybridization only genomic regions that cannot cross the species boundaries will show reciprocal monophyly. These regions, usually evolving rapidly under selection, are essential for the maintenance of species identity. I report discordant genealogical patterns and differential introgression rates across the genome. The most dramatic outliers, showing near zero introgression and more structured species trees, are also the only two seminal protein loci under selection. These are candidate barrier genes with possible reproductive functions. I also use the genealogical data to examine the demographic history and the current structure of the hybrid zone. iii BIOGRAPHICAL SKETCH Luana Santoro Maroja was born on the 19 th of October 1976 in Rio de Janeiro, Brazil. Growing up in the tropical Atlantic rain forest, Luana has always been fascinated with Biology. As a young child, she dreamed of becoming a "dinosaur LIST OF FIGURES x

Journal of Systematic Palaeontology

Spruce beetle, Dendroctonus rufipennis (Kirby), is one of the most broadly distributed bark beetl... more Spruce beetle, Dendroctonus rufipennis (Kirby), is one of the most broadly distributed bark beetles in North America, extending from Alaska to Newfoundland, south to Arizona. It colonizes most species of spruce within its range. Usually it is associated with highly stressed or killed trees, but under certain conditions undergoes landscape level eruptions that kill millions of trees (Werner and others 1977), regardless of their physiological condition (Wallin and Raffa 2004). Populations may be semivoltine or univoltine, depending on temperature (Hansen and others 2001). Spruce beetles show relatively close associations with several species of fungi (Six and Bentz 2003), some of which vary in frequency with beetle population phase (Aukema and others 2005). Adult beetles were collected from sixteen sites extending across the full range of D. rufipennis. DNA was extracted, and approximately 100 beetles were sequenced for mtDNA and approximately 550 beetles were genotyped for microsatellites (Maroja and others subm). Phylogenies were reconstructed by several means, including Maximum Parsimony and Bayesian Posterior approaches. We also computed isolation by distance, neutral evolution, migration and divergence time between populations, linkage disequilibrium, and deviation from Hardy-Weinberg equilibrium (Maroja and others 2007). Three distinct clades were apparent (Maroja and others 2007). Two are northern, extending west to east from Alaska to Newfoundland, and the third extends north to south throughout the Rocky Mountains. The Rocky Mountain clade further subdivides into northern and southern clades. A zone of overlap is located in southern British Columbia, which appears to represent secondary contact between beetles that moved north along the Rocky Mountains and beetles occupying the boreal forests of Canada. There is high among-clade divergence. Across all populations, there was a strong relationship between genetic distance and physical distance. This relationship was also significant within one northern clade. However, there was no isolation by distance effect within the other two clades, or within the pooled northern clades. There was no evidence for migration between the northern and southern Rocky Mountain clades. These same patterns segregate according to spruce species, and there is little evidence for migration between white and Engelmann spruce. However, host plant relationships cannot be teased apart from underlying geographic distribution patterns of tree species.

Hmel1-2_haploid and pacbio_haploid merged by HaploMerge

Hmel1-2 genome collapsed by HaploMerge

SQLite3 database containing marker information for linkage map (see README.txt for table descript... more SQLite3 database containing marker information for linkage map (see README.txt for table descriptions

Variant calls for Heliconius melpomene mapping cross aligned to Hmel1-1 primary scaffolds (Hmel1-... more Variant calls for Heliconius melpomene mapping cross aligned to Hmel1-1 primary scaffolds (Hmel1-1_primaryScaffolds.fa

Variant calls for Heliconius melpomene mapping cross aligned to Hmel1-1 haplotype scaffolds (Hmel... more Variant calls for Heliconius melpomene mapping cross aligned to Hmel1-1 haplotype scaffolds (Hmel_haplotype_scaffolds.fas

Variant calls for Eueides isabella cross aligned to Hmel2.f

FALCON PacBio assembly collapsed by HaploMerge

Initial assembly of PacBio reads with FALCO