Abstract
BackgroundSexual reproduction is a core biological function that is conserved throughout eukaryotic evolution, yet breeding systems are extremely variable. Genome-wide comparative studies can be effectively used to identify genes and regulatory patterns that are constrained to preserve core functions from those that may help to account for the diversity of animal reproductive strategies. We use a custom microarray to investigate gene expression in males and two reproductive stages of females in the crustacean Daphnia pulex. Most Daphnia species reproduce by cyclical parthenogenesis, alternating between sexual and clonal reproduction. Both sex determination and the switch in their mode of reproduction is environmentally induced, making Daphnia an interesting comparative system for the study of sex-biased and reproductive genes.ResultsPatterns of gene expression in females and males reveal that 50% of assayed transcripts show some degree of sex-bias. Female-biased transcription is enriched for translation, metabolic and regulatory genes associated with development. Male-biased expression is enriched for cuticle and protease function. Comparison with well studied arthropods such as Drosophila melanogaster and Anopheles gambiae suggests that female-biased patterns tend to be conserved, whereas male-biased genes are evolving faster in D. pulex. These findings are based on the proportion of female-biased, male-biased, and unbiased genes that share sequence similarity with proteins in other animal genomes.ConclusionSome transcriptional differences between males and females appear to be conserved across Arthropoda, including the rapid evolution of male-biased genes which is observed in insects and now in a crustacean. Yet, novel patterns of male-biased gene expression are also uncovered. This study is an important first step towards a detailed understanding of the genetic basis and evolution of parthenogenesis, environmental sex determination, and adaptation to aquatic environments.
Highlights
Sexual reproduction is a core biological function that is conserved throughout eukaryotic evolution, yet breeding systems are extremely variable
The coefficient of variation (CV) for spots combined across arrays ranged from 0.003–0.50, with a mean (± S.D.) of 0.04 ± 0.047 (n = 3,673), indicating a negligible effect of spot intensity on variation
We found no difference in codon usage bias between these classes as measured by frequency of optimal codons (Fop), codon bias index (CBI), codon adaptation index (CAI), or relative synonymous codon usage either at a four-fold cutoff, or at a more relaxed two-fold cutoff
Summary
Sexual reproduction is a core biological function that is conserved throughout eukaryotic evolution, yet breeding systems are extremely variable. Most Daphnia species reproduce by cyclical parthenogenesis, alternating between sexual and clonal reproduction Both sex determination and the switch in their mode of reproduction is environmentally induced, making Daphnia an interesting comparative system for the study of sex-biased and reproductive genes. Sex is a much stronger determinant of transcript levels than an animal's ontogeny [7], age, or genotype [10] These studies find that, overall, male-biased genes are evolving more rapidly than female-biased genes [9,13,14], providing evidence that males experience stronger positive selection than females [8,12]. Recent studies of Anopheles gambiae [3,16] report that a large proportion of gene expression is sex-biased and shows similar functional patterns to the female-biased gene set in flies. Further comparative experimental work is required to better understand the evolution of sex-biased gene expression
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