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Sex-specific differences in transcriptome profiles of brain and muscle tissue of the tropical gar

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The tropical gar fish or pejelagarto (Atractosteus tropicus) is a ray-finned chordate that inhabits the tropical freshwater habitats of the Caribbean and Pacific drainages, ranging from Southern Mexico to Northern Costa Rica [13]. The tropical gar is one of seven extant species that belong to the family Lepisosteidae, which consists of two genera of non-teleost bony fishes, Lepisosteus and Atractosteus, which diverged 100 million years ago [4]. The Lepisosteidae family of fishes are often referred to as “living fossils” because they belong to an ancient lineage in which most species are now extinct and extant species have experienced little evolutionary change for the past 100 million years [5]. The tropical gar is distinguished from other gars by its characteristic spotted, long, narrow body and snout, and average mature size of 50–60 centimeters [6]. Their preferred habitat is the slow moving waters of rivers and lakes, as well as backwaters and lagoons. They can survive in low oxygen levels and withstand moderately high water temperatures. The tropical gar is piscivorous [7], and reproduction occurs from March to November and peaks in July and August [8, 9]. In Mexico and Central America, there is a recreational fishing industry for tropical gar, and it is a popular food source due to its nutritional quality and low price. Tropical gar is one of the five main fishery resources in Mexico [13].

Because of the regional importance of the tropical gar, concerns about the wild population have arisen. Wild capture reached its peak in 1996, at 530.6 tons. However, in 1999, only 219 tons were captured [10]. No further analyses have been done to determine whether the decrease was due to population decline. The tropical gar has not been evaluated for conservation status by the International Union for Conservation of Nature (IUCN) Red List. Little is known about the species despite concerns about overexploitation by fisheries and habitat degradation caused by dam construction, oil extraction, urban expansion and agricultural expansion [9, 10]. Only one country, Costa Rica, has listed them as endangered [6]. Because of these concerns, several local agencies (for example, the Universidad Juárez Autónoma de Tabasco (UJAT), the Consejo Nacional de Ciencia y Tecnologia (CONACyT) and the Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA)) in Mexico and international agencies (for example, the United Nations Development Programme) are working to raise awareness and educate the public on ways to preserve their native aquatic resources [9, 11].

Interest in tropical gar aquaculture has increased to meet rising demand and to reduce pressure on wild populations. A barrier to breeding gar for food or research is that there is no easy way to differentiate males and females externally [9]. The challenge of distinguishing males from females is most accentuated during early and juvenile stages, whereas adult females are largely identifiable during the reproductive season by their prominent abdomen due to mature ovary development [8]. The only way to definitively distinguish males and females is through invasive procedures to identify whether an individual has ovaries or gonads. Additionally, varying ratios of females to males have been observed, with ratios of females to males as skewed as 1:10 in aquaculture settings [8, 9]. The genetic basis of sex determination in tropical gars has been inconclusive thus far due to the lack of differences in chromosome structure from karyotyping [12, 13] and the overall lack of genetic analyses. However, the skewed sex ratios may be due to an environmental sex determination mechanism, such as temperature-dependent sex determination, which has been identified as an important factor in determining sex ratios in many other species of fishes, amphibians, and reptiles [14].

In this study we examine sex-specific gene expression differences in adult tropical gar. Sex-specific differences have become increasingly evident across species and tissue types [1518]. Examining these sex differences at a molecular level is important in understanding structural, behavioral, and cellular differences between sexes. Additionally, these expression differences can lead to skewed disease risk between sexes [19]. Differences in gene expression between sexes has been shown to be relevant in human neurological diseases [15] and immune diseases, such as irritable bowel syndrome and allergy [20]. While gene expression differences between sexes can contribute to disease, there is also evidence that sexually dimorphic gene expression patterns are evolutionarily conserved and therefore also important to phenotypic differences between sexes [21].

In this study, the tropical gar transcriptome was assembled de novo. The assembled transcriptome was compared to the transcriptome of the spotted gar [22] and was also functionally annotated using existing databases. Ultimately, expression levels between muscle and brain tissue from three male and three female tropical gar were compared to identify sex-specific and highly differentiated transcripts.

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