Evolutionary Genomics of Panarthropoda: Study of the chemosensory gene families across phyla and the radiation of the spider genus Dysdera (Araneae, Dysderidae) in the Canary Islands

Abstract

[eng] During the last decade, advances in high-throughput sequencing (HTS) technologies have increased exponentially the generation of genomic data, especially of non-model species. In this thesis, we generated and used available HTS data to shed light on relevant evolutionary processes that shape genome structure and organization, such as the origin and evolution of multigene families, and the genomic determinants of adaptive radiations. First, we contribute to the genome assembly of the spider Dysdera silvatica, the first published assembly of a member of the Dysderidae family. For that we used a hybrid assembly strategy based on short (Illumina) and long (low coverage PacBio and Nanopore) reads to generate an assembly of moderate to low continuity (N50 of 38 kb). Then, we upgraded the assembly to a high quality, chromosome-level, using Chicago and Hi-C libraries, which raised the continuity of the previous draft considerably (N50 of 174.19 Mb). This newly generated genomic resource is not only a significant contribution to the field of spider genomics, but also the backbone for many of the analyses presented in this thesis. We identified 33,275 putative protein-coding genes in the genome of D. silvatica (87% of them were functionally annotated) and estimated that 52.87% of the genome are repetitive elements. We used this high-quality assembly to perform a comprehensive study of the chromosomal location and evolutionary divergence of chemoreceptor gene families. We identified 545 chemoreceptor genes, which are highly clustered in the genome of D. silvatica and show a clear correlation between physical and evolutionary distances. Second, we used available genomics data, and newly generated transcriptomes, to perform a phylogenetically deep study of the evolution of the chemosensory gene families across Panarthropoda. We characterized the expression of chemoreceptor genes in the antenna of the velvet worm Euperipatoides rowelli and performed a comparative genomic analysis of these gene families across representatives of the phyla composing the Panarthropoda clade. Noticeably, we did not find the expression of the Ionotropic co-receptor IR25a in onychophorans, which questions the chemosensory role of this family in this lineage. Surprisingly, eutardigrades lack genes encoding the DEG-ENaC and CD36/SNMPs gene families, a feature that could be related to their extraordinary resistance to desiccation. Finally, we propose the NPC2 gene family as the candidate chemosensory soluble protein in the Panarthropoda ancestor. We also used the chromosome-level assembly of D. silvatica to study some aspects of the adaptive radiation of the spider genus Dysdera in the Canary Islands. We performed a population genomics study of a natural population of D. silvatica from La Gomera using a whole-genome re-sequencing strategy. We found unexpected high levels of nucleotide polymorphism and a lower X/autosomes polymorphism ratio than the theoretically anticipated from their corresponding effective number of chromosomes. Demographic inference based on the coalescence predicted that in the past this species likely underwent a long period characterized by a large effective population size (about 100 times greater than the estimate for the present). We hypothesize that the high levels of polymorphism currently observed in the population of D. silvatica is the molecular hallmark of a long period of ancestral population structure that dominated the history of this species for almost 200 Kya. Globally, our results provide very valuable new knowledge about the genomic bases of adaptation at different evolutionary timescales, ranging from the deep evolutionary dynamics of chemosensory repertories across Panarthropoda phyla, to the very recent origin of new copies and the early steps of their evolution within a genome, including the genomic signals of positive selection and demographic history at the scale of an adaptive radiations. This thesis also demonstrates the great advantage of having highly continuous genome assemblies to obtain reliable data when working gene families, and other repetitive elements, or to perform comprehensive chromosome-level population genomics analyses.

[cat] Durant la darrera dècada, els avenços en les tecnologies de High- Throughput Sequencing (HTS) van augmentar exponencialment la generació de dades massives, proporcionant una gran quantitat d'informació genòmica d'espècies no models. L'objectiu principal d'aquesta tesi és investigar processos evolutius com l'origen i l'evolució de les famílies de gens i els mecanismes genòmics subjacents a l'adaptació en la diversificació d'espècies. Per això, en primer lloc, hem contribuït a la construcció de l’assemblatge genòmic de l’aràcnid Dysdera silvatica, el primer genoma de la família Dysderidae amb lectures curtes, amb una petita fracció de lectures llargues i un valor N50 de 38 kb. A continuació, el vam millorar a un genoma a nivell de cromosoma d'alta qualitat, utilitzant llibreries de Chicago i Hi-C, a més d'augmentar el valor de N50 a 174,19 Mb. Vam identificar 33.275 gens (el 87% amb anotacions funcionals), i determinar que el 52,87% del genoma estava representat per elements repetitius. Vàrem identificar 545 gens quimioreceptors, el 54% d'ells distribuïts en 83 clústers genòmics que es trobaven majoritàriament en els scaffolds més petits. D'altra banda, hem estudiat i caracteritzat les famílies multigèniques quimiosensorials a diverses espècies dels grup dels Panarthropoda, centrant-nos en Onychophora i Tardigrada. Hem caracteritzat les principals famílies quimiosensorials de l'onicòfor Euperipatoides rowelli i hem trobat que no tenen el gen que codifica el receptors ionotròpic IR25a, present en la majoria d’espècies de Protòstoms. A més, les famílies de gens DEG-ENaC i CD36/SNMPs són absents a les espècies de la classe Eutardigrada, mentre que la família de gens NPC2 seria l'única que codifica proteïnes solubles en l'ancestre Panartropoda. Finalment, hem estudiat la radiació adaptativa de l’aranya del gènere Dysdera a les Illes Canàries, mitjançant una anàlisi de genòmica de poblacions. Hem determinat que a pesar de ser una espècie endèmica i que viu a illes molt petites, presenta un alt nivell de polimorfisme nucleotídic. Les inferències demogràfiques suggereixen que aquesta espècie té una gran grandària efectiva poblacional, probablement causada per una estructuració poblacional ancestral. Els resultats d'aquesta tesi són un recurs valuós que ens ha permès caracteritzar detalladament les famílies multigèniques del sistema quimiosensorial, a més proporcionar nou coneixement sobre paper relatiu de la selecció positiva en les radiacions adaptatives.