Osiris Genes and Insect Adaptive Evolution

Abstract

The Osiris gene family is unique to insect lineages. Though the exact function of Osiris genes has remained elusive, recent work has furthered our understanding of their critical role in insect development, adaptation and likely speciation. Insects are among the most evolutionarily successful groups, and important aspects of their biology are regulated by or associated with Osiris gene expression. Most insect genomes contain 20–25 Osiris genes which reveal remarkable conserved synteny and sequence homology across hundreds of millions of years. Given the essential nature of Osiris genes in insect development, we consider this gene family understudied. While their molecular function is as of yet unclear, their importance in insect evolution is now just coming to light. Osiris genes have a function in phenotypic plasticity, metabolisim, and immunity, making them key targets of selection as well as for insect population control.

Key Concepts

  • Osiris gene family expansion occurred early in insect evolution.
  • Osiris genes have conserved synteny across hundreds of millions of years.
  • Osiris genes are essential in development, are correlated in expression.
  • At least some Osiris genes are involved in endosomal trafficking.
  • Osiris genes are involved in adaptive processes, such as phenotypic plasticity, immunity, and detoxification.

Keywords: gene family; synteny; metabolism; plasticity; immunity

Figure 1. A diagram of gene family expansion by unequal crossing over. A chromosomal segment from an ancestral organism is shown with genes A, B and C indicated. Out‐of‐register recombination during meiosis can lead to tandem duplication of a chromosomal segment containing the B gene (the other product would be a deletion of the B gene, chromosome not shown). After a period of divergence, B1 and B2 become distinct genes, members of the B gene family. Additional rounds of unequal crossing over followed by divergence lead to further gene family expansion (or contraction when genes are deleted by this same process). A phylogenetic relationship among the B gene family members can be reconstructed as shown using analysis of gene sequences.
Figure 2. Phylogenetic relationships among Osiris gene family members (adapted from (Smith et al., )) and relationships among insects. The table where the two phylogenies converge shows the gene copy number for each taxon. Gene copy number is colour coded to highlight genes that have undergone lineage‐specific expansions. Major Osiris gene groups are colour coded in the gene phylogeny and match the colours in Figure (synteny).
Figure 3. A schematic of Osiris gene synteny across three insect taxa, the fruit fly (D. melanogaster, top), the honey bee (A. mellifera, middle) and the flour beetle (T. castaneum, bottom). Individual Osiris genes are symbolised by coloured boxes where the colours correspond to evolutionary groupings from Figure . For context, their approximate positions on chromosomes/linkage groups are also shown. Some of the historic synteny of T. castaneum was disrupted by both an ∼3 Mbp translocation (Osi14‐16) and a chromosomal inversion (Osi1‐11). The conservation of synteny between bees and flies/beetles has existed for approximately 345 Ma, and between beetles and flies for 327 Ma (Misof et al., ).
Figure 4. Osiris genes are expressed in different tissues throughout insect development. (a) From an in situ hybridisation study detecting mRNA for each Osiris gene in the fruit fly (D. melanogaster) embryo (Ando et al., PMID: 31006566), Osi4 is expressed broadly in the epidermis (dark green). Osi6 and Osi7 are expressed in epidermal stripes along denticle belts (light green), and Osi1, Osi2, Osi3, Osi5, Osi8, Osi9, Osi11, Osi13, Osi15, Osi17, Osi18, Osi19, Osi20, Osi21, Osi22, Osi23 and Osi24 are expressed in the trachea (red) (b) From insect larval studies (depicted as an L3 Drosophila larvae) Osi9 is highly expressed in the larval silk gland (pink (Royer et al., ; Liu et al., )). Osi7, Osi18, Osi19, Osi9‐1, Osi9‐2, Osi9‐3 and Osi9‐4 are upregulated in the B. mori midgut after an ecdysone stimulated larval‐to‐larval moulting (orange (Yang et al., )). In the black dilute (bd) mutant, B. mori larva, Osi8, Osi9, Osi17, Osi19, Osi20 and Osi21 are upregulated in the integument (light blue (Wu et al., )). (c) In the fruit fly (D. melanogaster) pupae, Osi1, Osi3, Osi4, Osi7, Osi8, Osi9, Osi11, Osi12 and Osi22 are highly expressed at 42 h APF in the pupal wing (blue (Sobala and Adler, )). An RNA‐sequencing study quantifying gene expression in different tissues throughout D. melanogaster development shows moderate to very high expression of Osi1, Osi3, Osi4, Osi6, Osi7, Osi9 and Osi12 in the pupal central nervous system (green) and moderate to extremely high expression of Osi1, Osi2, Osi3, Osi4, Osi6, Osi7, Osi8, Osi9, Osi12, Osi14, Osi15, Osi19, Osi20, Osi21 and Osi22 in the pupal fat body (Graveley et al., ). (d) In the adult fruit fly (D. melanogaster), Osi6 is moderately expressed in the 20‐day adult digestive system and moderately high in the adult virgin 20‐day old head (yellow (Graveley et al., )). In the adult eye (green), Osi21/diehard regulates the degradation of endocytosed rhodopsin (Lee et al., ). Osi23/gore‐tex is involved in nanopore formation in the Drosophila olfactory sensillum (blue (Ando et al., )) Drosophila images adapted from Hartenstein, , Atlas of Drosophila Development.
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Coolon, Joseph D, Drum, Zachary, Lanno, Stephen M, and Smith, Chris R(Oct 2019) Osiris Genes and Insect Adaptive Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028763]