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Insights from the Genome of Melitaea Cinxia

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Insights from the Genome of Melitaea Cinxia Ann. Zool. Fennici 54: 275–291 ISSN 0003-455X (print), ISSN 1797-2450 (online) Helsinki 15 May 2017 © Finnish Zoological and Botanical Publishing Board 2017 Ilkka Hanski: The legacy of a multifaceted ecologist Butterfly genomics: insights from the genome of Melitaea cinxia Virpi Ahola1, Niklas Wahlberg2 & Mikko J. Frilander3,* 1) Department of Biosciences, P.O. Box 65, FI-00014 University of Helsinki, Finland 2) Department of Biology, Lund University, Sölvegatan 37, SE-223 62 Lund, Sweden 3) Institute of Biotechnology, P.O. Box 56, FI-00014 University of Helsinki, Finland (*corresponding author’s e-mail: [email protected]) Received 2 Dec. 2016, final version received 9 Feb. 2017, accepted 9 Feb. 2017 Ahola, V., Wahlberg, N. & Frilander, M. J. 2017: Butterfly genomics: insights from the genome of Melitaea cinxia. — Ann. Zool. Fennici 54: 275–291. The first lepidopteran genome (Bombyx mori) was published in 2004. Ten years later the genome of Melitaea cinxia came out as the third butterfly genome published, and the first eukaryotic genome sequenced in Finland. Owing to Ilkka Hanski, theM. cinxia system in the Åland Islands has become a famous model for metapopulation biology. More than 20 years of research on this system provides a strong ecological basis upon which a genetic framework could be built. Genetic knowledge is an essential addition for understanding eco-evolutionary dynamics and the genetic basis of variability in life history traits. Here we review the process of the M. cinxia genome project, its implica- tions for lepidopteran genome evolution, and describe how the genome has been used for gene expression studies to identify genetic consequences of habitat fragmentation. Finally, we introduce some future possibilities and challenges for genomic research in M. cinxia and other Lepidoptera. Enter genomics colonization (Wheat et al. 2011, Somervuo et al. 2014, Kvist et al. 2015). The genomic revo- The past four decades have been a time of lution in insects started with the publication of unprecedented progress in biological sciences, the Drosophila melanogaster genome in 2000 to which Ilkka Hanski made fundamental contri- (Adams et al. 2000), which itself was a prelude butions. His insights into the causes and conse- to the human genome project. This huge project quences of population dynamics at the ecological demonstrated that it is technically possible to level paved the way for a more intimate look at delve into the genomes of complex eukaryotes how the dynamics and the evolutionary history and discover the genetic mechanisms behind of a species are reflected at the genomic level. various life history traits. About four years later, In the last two decades, this intimacy advanced the genomic revolution reached Lepidoptera, from allele frequency studies of a single genetic with a draft silkworm (Bombyx mori) genome marker (Orsini et al. 2009, Hanski 2011) to a being published by two competing groups (Mita full-blown genomic scale investigation to iden- et al. 2004, Xia et al. 2004). This and the rapid tify the specific genes involved in dispersal and development of sequencing technologies set off 276 Ahola et al. • ANN. ZOOL. FENNICI Vol. 54 the race to sequence the first butterfly genome, set of studies on the ecology, evolution and and the main finalist contenders appeared to be genetics of this species. Ilkka Hanski and col- Hanski’s M. cinxia, as well as Heliconius mel- leagues have made substantial contributions to pomene and Bicyclus anynana, each of which the development of metapopulation theory using had been extensively used as model systems to the system (Hanski 1999, Hanski & Ovaskainen study different aspects of biology. 2000), but also for other ecological investiga- Through the subsequent years, researchers tions at the landscape scale (Hanski & Saccheri followed the progress of the three competing 2006, Hanski 2011). projects at various conferences and were all The development of next generation sequenc- surprised when the first butterfly genome to be ing (NGS) has enabled individual research published was the monarch butterfly (Danaus groups studying the ecology of natural popu- plexippus) (Zhan et al. 2011). The Heliconius lations to expand their scope to investigate the melpomene genome followed soon after (The genetic and molecular basis of individual fitness Heliconius Genome Consortium 2012), and the traits at the scale of the whole genome. Thus M. cinxia genome two years later (Ahola et al. the technological development has changed the 2014). At present, there are 25 published Lepi- entire research field from predominantly hypoth- doptera genomes of which 18 represent differ- esis-driven approaches with a small number of ent butterfly species (NCBI database accessed candidate genes to more hypothesis-free global November 2016). This genomic revolution approaches that can help to understand popula- has set the stage ready for investigations on tion-level phenomena such as local adaptation genome-environment interactions on ecologi- or population dynamics at the genomic level. cally well-studied species. For genetic research relying on genetic mark- Ilkka Hanski’s dream of sequencing the ers, NGS has been a tremendous help, enabling genome of his favorite species was realized in efficient and large-scale marker discovery. The time for him to be able to actively start integrat- benefits of NGS are particularly true in Lepi- ing the population biology and genomics of his doptera research, for which it has been difficult favorite species. Here we review the process to develop microsatellite markers (Van’t Hof of obtaining the whole genome sequence and et al. 2007) — the probable reason why only a highlight the published results as well as discuss few studies using genetic markers existed for future possibilities and challenges. Lepidoptera prior to the genomic revolution. At the more technical front, the access to whole genome or transcriptome sequences has signifi- Why was the Melitaea cinxia cantly accelerated development and implementa- genome important? tion of the custom genotyping arrays that in turn allow simultaneous screening of a large number The Glanville fritillary butterfly (Melitaea of different genetic markers for a large number of cinxia) model system in the Åland Islands in individuals. Therefore, the possibilities offered Finland was originally developed to study the by the new technologies were exciting, prom- effects of habitat fragmentation (Ehrlich & ising a rational selection of (a large number of) Hanski 2004). The system represents a classic genetic markers in contrast to the semi-arbitrary metapopulation consisting of ca. 4000 habitat process of candidate gene selection. patches of dry meadows that can be divided into The motivation for genomic studies of the 131 networks (Ojanen et al. 2013). Movement Glanville fritillary arose not only from the aims within networks is common, but long migration to find association between genotypic and phe- distances make such movements rare between notypic variation in general, but from the special the networks. The annual large-scale survey interest to understand the genetic basis of female of the whole metapopulation has formed the reproductive success and dispersal related traits, backbone of these studies, which, coupled with both of which are essential for the species to per- experiments in common garden conditions and sist in fragmented landscapes. It was important outdoor cages, have enabled a large and diverse to define the genetic and molecular level impact ANN. ZOOL. FENNICI Vol. 54 • Insights from the genome of Melitaea cinxia 277 of variation in dispersal traits but also the role of discussed elsewhere in this issue (Niitepõld & natural selection for population and evolutionary Saastamoinen 2017). dynamics in the study system. Additionally, the genomic resources enable building a pedigree across the entire Åland Islands study system The trials and tribulations of over several generations. Such a pedigree could building the Melitaea cinxia be used for obtaining empirical assessments genome of dispersal and gene flow, but most impor- tantly, for eco-evolutionary dynamics modeling The idea for sequencing the whole genome of with special interest in population growth and M. cinxia was initially born around 2006, before inbreeding depression. the first NGS platforms became available, but More than 20 years of research on the study was at that time regarded as a “dream project”. system has provided plenty of material and The justification for the dream was that it would examples of quantitative and qualitative vari- open the door to many genomics tools that ables that appeared to have a genetic basis, were available for laboratory model organisms and can be linked to the landscape level. For but which required full genome sequence. The instance, on the Åland Islands, female Glanville dream started to become attainable in 2006 when fritillary use two plant species, Plantago lanceo- the first NGS technology, 454 pyrosequencer lata and Veronica spicata, during oviposition as (launched in 2005), landed at the Institute of hosts for larvae (Nieminen et al. 2004). Earlier Biotechnology (BI), University of Helsinki. studies have suggested that female oviposition Soon after publishing the M. cinxia transcrip- preference on one of the host plant species is tome sequence using 454 sequencing technology genetically determined (Kuussaari et al. 2000, (Vera et al. 2008), the decision for sequencing Hanski & Singer 2001). Oviposition
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