Preadult life history variation determines adult transcriptome expression

Abstract

Preadult determinants of adult fitness and behaviour have been documented in a variety of organisms with complex life cycles, but little is known about expression patterns of genes underlying these adult traits. We explored the effects of differences in egg-to-adult development time on adult transcriptome and cuticular hydrocarbon variation in order to understand the nature of the genetic correlation between preadult development time and premating isolation between populations of Drosophila mojavensis reared in different host cactus environments. Transcriptome variation was analysed separately in flies reared on each host and revealed that hundreds of genes in adults were differentially expressed (FDR P < 0.05) due to development time differences. For flies reared on pitaya agria cactus, longer preadult development times caused increased expression of genes in adults enriched for ribosome production, protein metabolism, chromatin remodelling and regulation of alternate splicing and transcription. Baja California flies reared on organ pipe cactus showed fewer differentially expressed genes in adults due to longer preadult development time, but these were enriched for ATP synthesis and the TCA cycle. Mainland flies reared on organ pipe cactus with shorter development times showed increased transcription of genes enriched for mitochondria and energy production, protein synthesis and glucose metabolism: adults with longer development times had increased expression of genes enriched for adult life span, cuticle proteins and ion binding, although most differentially expressed genes were unannotated. Differences due to population, sex, mating status and their interactions were also assessed. Adult cuticular hydrocarbon profiles also showed shifts due to egg-to-adult development time and were influenced by population and mating status. These results help to explain why preadult life history variation determines subsequent expression of the adult transcriptome along with traits involved with reproductive isolation and revealed previously undocumented connections between genetic and environmental influences over the entire life cycle in this desert insect.

Keywords: cactus; cuticular hydrocarbons; development time; gene expression; life cycle; microarrays; transcriptome.

Figure 1

Diagram of the design of this experiment. Each population was reared on fermenting host cacti, and eclosed adults were grouped by day of development time. Males and females were aged to sexual maturity, 9 days for females and 13 days for males, in vials containing laboratory food. They were either stored separately or combined with an equal number of members of the opposite sex for 24 hours. From each of the 16 treatment groups, adults were frozen for CHC analysis or flash frozen in liquid nitrogen for RNA extraction in groups of 24 adults. Some replicates of organ pipe cactus-reared, mated, mainland adults were missing, see text for details.

Figure 2

Change in total CHCs per aged adult fly with egg to adult development time. Regression equations for mainland, Las Bocas adults were: mated (NS) y = − 79.5x + 1075.9, r² = 0.08; virgin (P < 0.05) y = −33.6x + 967.3, r² = 0.05; Baja California, Punta Prieta: mated (NS) y = 58.1x + 405.5, r² = 0.07; virgin (P < 0.05) y = 188.5x* −25.9x²* + 435.7, r²= 0.05. Terms in parentheses indicate regression model significance, NS =- not significant, * P < 0.05 for individual regression terms.