Phylogenomics identifies an ancestral burst of gene duplications predating the diversification of aphidomorpha

Abstract

Large-scale gene duplication, including whole-genome duplication (WGD), is a very common phenomenon in eukaryotic genomes. Bursts of gene duplications are considered a major source of evolutionary innovation and have been associated with the increase in biological complexity and adaptive radiations of species (Zhang 2003). In particular, large-scale gene duplications, generally associated with WGDs, have been reported for many eukaryotic lineages including plants (Van de Peer et al. 2017), fungi (Marcet-Houben and Gabaldón 2015), and animals (Taylor et al. 2001). Although large-scale duplication seems less pervasive in animals than in plants, a growing number of studies report such events in animals. Among other lineages, putative WGDs have been described at the base of vertebrates (Ohno 1970; Dehal and Boore 2005; Putnam et al. 2008), and in several lineages of fish (Christoffels et al. 2004; Glasauer and Neuhauss 2014), amphibians (Mable et al. 2011; Session et al. 2016), and arthropods (Jacobson et al. 2013; Kenny et al. 2016; Schwager et al. 2017; Li et al. 2018).

Aphids belong to the infraorder Aphidomorpha that includes three families: Aphididae, Adelgidae, and Phylloxeridae (Favret 2013; Nováková et al. 2013; Blackman and Eastop 2000). Aphids and related (Aphidomorpha) species (Becker-Migdisova and Aizenberg 1962) are hemipteran insects that feed on plant sap (Tjallingii 1995). This specialized diet, rich in carbohydrates but poor in nitrogen compounds, has resulted in several adaptations including the establishment of tight relationships with bacterial endosymbionts (Scarborough et al. 2005; Moya et al. 2008; von Dohlen et al. 2017). There are more than 5,000 described aphid species, of which, about 450 have been collected from crop plants, and 100 are considered of significant economic importance (Van Emden and Harrington 2017). Genomes of several aphid species of agricultural interest have been sequenced, including Acyrthosiphon pisum, Myzus persicae, Diuraphis noxia, Aphis glycines, and Sipha flava (International Aphid Genomics Consortium 2010; Nicholson et al. 2015; Mathers et al. 2017; Wenger et al. 2017). However, except for S. flava (subfamily Chaitophorinae), the sequenced aphids belong to a single subfamily, Aphidinae, limiting our understanding of the genomic diversity in this group of insects. Remarkably, most genome analyses in these species have revealed an important number of paralogous sequences and expanded gene families, including amino acid transporters, odorant and gustatory receptor genes, miRNA-specific dicer-1, ago1 genes, and pasha, among others (Smadja et al. 2009; Huerta-Cepas et al. 2010; Jaubert-Possamai et al. 2010; Duncan et al. 2016; Mathers et al. 2017). However, the close relatedness of the sequenced species provides little resolution to the phylogenetic placement of the duplication events, particularly the ancestral ones.

Recent studies have focused on assessing patterns of sequence and expression divergence among recently duplicated genes in A. pisum (Fernández et al. 2019) or M. persicae (Mathers et al. 2017). They have also inspected the distribution of old and young A. pisum paralogs along chromosomes, by categorizing the age of genes that are best-reciprocal hits of each other based on the amount of synonymous substitutions (Li et al. 2019). However, we still lack a proper understanding of when the ancestral duplications occurred, and whether they can be linked to phenotypic innovations shared by aphids or related species. To better assess the origin of the paralogous genes of aphids we sequenced the genome of Cinara cedri (Lachninae subfamily, tribe Eulachnini), the first representative genome from an early-branching lineage of the Aphididae family. Cinara species (and most Lachninae) are particular among aphids as they feed on conifers (gymnosperms), whereas all the other genome-sequenced aphids feed on angiosperms. Another clear difference between the Lachninae and the rest of aphids is that two co-obligate endosymbionts (Buchnera aphidicola, Serratia symbiotica) are present in this group, whereas only B. aphidicola is obligate for the rest of aphids (Latorre and Manzano-Marín 2017). We used a phylogeny-based approach (Huerta-Cepas and Gabaldón 2011) to provide the relative timing of aphid duplications in a phylogenetic framework that includes 21 other fully sequenced genomes and two transcriptomes. Our results provide compelling evidence for an ancestral wave of gene duplications, whose origin predates the diversification of all sequenced aphids, adelgids, and phyloxerids, but are subsequent to their divergence from the Coccoidea lineage, ∼106–227 Ma.

This research was funded by European Regional Development Fund (ERDF) and Ministerio de Economía y Competitividad (Spain) (Grant Nos. PGC2018-099344-B-100 and BFU2015-67107). T.G. group also acknowledges support from the Catalan Research Agency (AGAUR) SGR857, and grants from the European Union’s Horizon 2020 research and innovation program under the grant agreements ERC-2016-724173 and MSC-747607. T.G. also receives support from an INB (Grant No. PT17/0009/0023—ISCIII-SGEFI/ERDF). The authors want to thank Sophia Derdak for her help in the genome polishing step.

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