Sexually Dimorphic Gene Expression in the Lateral Eyes Of
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Sajuthi et al. EvoDevo (2015) 6:34 DOI 10.1186/s13227-015-0026-2 RESEARCH Open Access Sexually dimorphic gene expression in the lateral eyes of Euphilomedes carcharodonta (Ostracoda, Pancrustacea) Andrea Sajuthi1,2, Brenna Carrillo‑Zazueta1,3, Briana Hu1, Anita Wang1,4, Logan Brodnansky1,4, John Mayberry1 and Ajna S. Rivera1* Abstract Background: The evolution and development of sexual dimorphism illuminates a central question in biology: How do similar genomes produce different phenotypes? In an XX/XO system especially the state of a sexually dimorphic trait is determined by differences in gene expression, as there are no additional genetic loci in either sex. Here, we examine the XX/XO ostracod crustacean species Euphilomedes carcharodonta. This species exhibits radical sexual dimorphism of their lateral eyes, females have only a tiny simple lateral eye while males have elaborate ommatidial eyes. Results: We find that males express three of nine eye-development gene homologs at significantly higher levels dur‑ ing juvenile eye development, compared to females. We also find that most eye-development genes examined are pleiotropic, with high expression levels during embryonic development as well as during juvenile eye development. Later, in adults, we find that phototransduction genes are expressed at higher levels in males than in females, as we might expect when comparing ommatidial to simple eyes. Conclusions: We show here that expression changes of a handful of developmental genes may underlie the radical difference in a dimorphic character. This work gives an important point of comparison for studying eye evolution and development in the Pancrustacea. Keywords: Sexual dimorphism, Evolution, Development, Eye, Expression, Pancrustacean, Ostracod Background of different sexes? Recent studies focused on the global In recent years, the genetics underlying sex determina- expression differences in males and females have found tion have been under close scrutiny. Deep homology has hundreds to thousands of genes expressed in a sexually been found at the heart of the diverse regulatory systems dimorphic fashion [2–4]. On a different scale, other stud- underlying sex determination in disparate animals [rev. ies have uncovered the expression differences in a single in 1]. However, the output of these gene regulatory net- gene underlying fate choice of a bipotential tissue, finding works, the genetic underlying specific sexually dimorphic that dimorphic expression is key to fate determination traits, has been more elusive. Studying sexual dimor- [5–8]. phism at the genetic level allows us to ask two intriguing The second question is an evolutionary one: How does questions. First, in determining a dimorphic character, dimorphism evolve at the genetic level, and how are two how does a single set of genes found within the same phenotypes maintained in a single species? The evolu- species produce multiple phenotypes among individuals tion of dimorphism has been studied at the genetic level in other organisms and has led to gains in understanding *Correspondence: [email protected] both the genetics of trait evolution as well as the genetic 1 Department of Biological Sciences, University of the Pacific, Stockton, basis of convergence. Work on the Drosophila pigmenta- CA, USA tion gene bric-a-brac (bab) has revealed an evolutionary Full list of author information is available at the end of the article © 2015 Sajuthi et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sajuthi et al. EvoDevo (2015) 6:34 Page 2 of 14 scenario for changes in axial patterning. In this case, selection, wherein males and females occupy different ancestral monomorphic expression evolved into a dimor- visual environments with different selective pressures phic pattern via complex changes in cis-regulatory ele- [21]. Evidence for this was found in a previous predation ments regulated by the axial patterning gene abd-B and study where male Euphilomedes were found to be pre- the sex-determination gene doublesex (dsx) [6]. Another dated on at a higher rate when their eyes were obscured, group of insects, butterflies, also have species with sexu- while female Euphilomedes were not [21]. Observational ally dimorphic pigmentation patterning. In the case of studies on related species find that males spend more time Heliconius, the gene expression difference in optix that in the water column and females spend more time in the underlies the dimorphism in H. doris also underlies much sand where they are not accessible to predators [22, 23]. morphological diversity among the genus [9]. The genetic Arguing against sexual selection driving the dimorphism link between sexual dimorphism and macroevolution is is the finding that male visual acuity does not appear to not limited to insects, recent studies on cichlid fish have allow for detection of females, sectioned adult male eyes shown that sexually dimorphic craniofacial morphology have an interommatidial angle of 8° corresponding to a is similar to interspecies variation and may have a similar sensitivity of 2.3 µm2 ċsteradian [21]. Given these calcula- developmental basis [10, 11]. tions, in bright clear water Euphilomedes males would be Pancrustacean eyes are a particularly useful case for able to detect females at a range of 12 mm or less, while studying the evolution and development of eyes at the they would be able to detect juvenile fish predators (1 cm genetic level. Not only do they exhibit the largest num- in length) at a range of 7.1 cm [21]. Together, these find- ber of optical types of all animal groups [12] but they also ings suggest a scenario where selection for image-forming have a large number of genetic tools available and a model eyes in males may be driven by their more predator-rich genetic organism to compare findings to, Drosophila. niche while selection against image-forming eyes, or neu- Moreover, unlike other examples of sexual dimorphism tral drift, in females may be driven by the higher energetic informing macroevolution, compound eyes in Pancrus- cost of building and maintaining eye tissue. Indeed, eye tacea are complex structures; understanding the genetics reduction has been found in many species living in light- underlying eye diversity can deepen our understanding poor environments, for example caves [24], and has been of eye evolution in general. Currently, the evolution of seen in particular in abyssal myodocopid ostracods [25, image-forming eyes in arthropods is an unresolved topic 26]. Thus, if eye degeneration is seen as the default state in biology. Phylogenetic, developmental, and morpholog- in the absence of visual data, the ecological significance ical approaches have led to competing theories regard- of the different Euphilomedes eye types may mirror selec- ing eye homology and evolutionary trajectories in each tive pressures driving the evolution of compound eyes. A lineage [13–15]. The availability of transcriptomics and similar scenario has been proposed for Lake Malawi cich- gene expression techniques for non-model arthropods is lid fish, where craniofacial sexual dimorphism mirrors a boon to this topic and have been used to find homol- differences in ecomorphs. In both the fish and ostracods, ogy in eye development and phototransduction in several the genetics underlying ecologically driven sexual dimor- arthropod taxa [16–19]. A recent project comparing eye phism may very well also underlie variation between spe- morphology in two populations of isopods—one cave cies [11]. and one surface population—used QTL analysis com- Second, the evolutionary history of dimorphism in sar- bined with a candidate gene approach to map loci associ- sielloid ostracods may be complex with multiple losses ated with both eye and pigmentation loss [20]. Sarsielloid and gains in different lineages. Studying dimorphism in ostracod crustaceans (Myodocopida) provide another one species will give us target genes to examine in study- approach to comparing development of eye types. Sev- ing the evolution of convergence. On a more practi- eral species of sarsielloids are sexually dimorphic—males cal note, eye differentiation happens externally during have large image-forming eyes while females have only juvenile stages, making the eyes accessible for dissec- rudimentary eyes that lack ommatidia. While QTL analy- tion and observation (Fig. 1). Finally, Euphilomedes has sis would be difficult on these organisms, there is a pub- been shown to have XO/XX sex determination (as have lished transcriptome for Euphilomedes carcharodonta other ostracod species) [27–30]. This eliminates the juvenile male eyes from which candidate dimorphically possibility that eye-development genes are present on a expressed genes can be drawn [21]. E. carcharodonta male-specific chromosome. Because of this, male/female eye dimorphism in particular is a promising subject for differences in eye development must be regulated at the understanding the evolution, development, and genetics gene expression level,