[OANNES Foro] The seahorse genome and the evolution of its specialized morphology

Jue Dic 15 08:23:57 PST 2016

Nature 540, 316

(15 December 2016)

doi:10.1038/540316a

A Nature paper explores this unusual creature from the inside out.

Sequence reveals genes behind bizarre sea-horse traits

14 December 2016

http://www.nature.com/news/sequence-reveals-genes-behind-bizarre-sea-horse-traits-1.21149?WT.ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2

The gods of Greek mythology were busy people. Poseidon, as well as having dominion over the sea and sending earthquakes, had a sideline in creating animals. His most celebrated design was the horse. Poseidon was so keen on his horses that he held onto some to pull his chariot through the waves. These first sea horses — called the hippocampi or, loosely, horse-monsters — had the tails of fish and two front hooves. They could be seen on a windy day, racing across the foam and waves of the sea’s surface. That’s why ocean breakers are still called white horses.

The sea horse, in other words — or its name at least — has a complicated origin story. Whereas Poseidon’s mythical horses were considered the most beautiful creatures of the ancient world, the real sea horse has a tale of wonder of its own to tell. These fragile, elegant animals look like almost nothing else on Earth (except, naturally, a horse, and a distinctive part of the human brain). They are fish without scales and the usual fins. They are covered in bony plates. They swim upright. They form monogamous pairs. And most famously, the male sea horse experiences pregnancy — well, the closest that fish get to pregnancy — as he holds and nurtures the developing embryo in a special pouch.

In a paper this week, scientists explore the bizarre features of the sea horse from the inside out ( <http://www.nature.com/uidfinder/10.1038/nature20595> Q. Linet al. Nature 540, 395–399; 2016). They describe how they sequenced and analysed the genome of Hippocampus comes, the tiger tail sea horse (just to add to the morphological mix). The results offer some clues to the genetic basis of their unique traits.

A gene family with a role in embryo hatching shows high expression in the male brood pouch, the scientists say. And some potential regulatory elements are missing, which might help to explain the evolution of the sea horse’s strange body shape. The animals eat through a tubular snout (no teeth) and, sure enough, the genome showed a lack of genes for enamel proteins, needed to make teeth. The absence of a gene called tbx4, a known regulator of limb development, may have contributed to the loss of pelvic fins. And to the unusual features of the sea horse we can add a relatively high evolutionary rate in their genes as compared to other fish.

As we gain understanding of what makes the sea horse so special, its future is far from assured. Many of the 46 or so known species are on the endangered list: drained from the sea as by-catch and sent around the world as live pets or as dried food and medicine. The sea horse is a powerful symbol, and one that has been used to catalyse conservation efforts, such as the creation of protected marine zones in places such as the Philippines. But pollution and habitat loss are also taking their toll —  as they are on much of the wider ocean environment. The white horses may still skim across the surface, but the world of Poseidon is losing its magic.

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Nature 540, 395–399

(15 December 2016)

doi:10.1038/nature20595

Published online 14 December 2016

The seahorse genome and the evolution of its specialized morphology

·          <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-1> Qiang Lin,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-2> Shaohua Fan,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-3> Yanhong Zhang,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-4> Meng Xu,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-5> Huixian Zhang,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-6> Yulan Yang,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-7> Alison P. Lee,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-8> Joost M. Woltering,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-9> Vydianathan Ravi,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-10> Helen M. Gunter,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-11> Wei Luo,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-12> Zexia Gao,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-13> Zhi Wei Lim,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-14> Geng Qin,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-15> Ralf F. Schneider,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-16> Xin Wang,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-17> Peiwen Xiong,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-18> Gang Li,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-19> Kai Wang,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-20> Jiumeng Min,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-21> Chi Zhang,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-22> Ying Qiu,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-23> Jie Bai,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-24> Weiming He,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#auth-25> Chao Bian 

Abstract

Seahorses have a specialized morphology that includes a toothless tubular mouth, a body covered with bony plates, a male brood pouch, and the absence of caudal and pelvic fins. Here we report the sequencing and de novo assembly of the genome of the tiger tail seahorse, Hippocampus comes. Comparative genomic analysis identifies higher protein and nucleotide evolutionary rates inH. comes compared with other teleost fish genomes. We identified an astacin metalloprotease gene family that has undergone expansion and is highly expressed in the male brood pouch. We also find that the H. comes genome lacks enamel matrix protein-coding proline/glutamine-rich secretory calcium-binding phosphoprotein genes, which might have led to the loss of mineralized teeth. tbx4, a regulator of hindlimb development, is also not found in H. comes genome. Knockout of tbx4 in zebrafish showed a ‘pelvic fin-loss’ phenotype similar to that of seahorses.

Members of the teleost family Syngnathidae (seahorses, pipefishes and seadragons) ( <http://www.nature.com/nature/journal/v540/n7633/fig_tab/nature20595_SF1.html> Extended Data Fig. 1), comprising approximately 300 species, display a complex array of morphological innovations and reproductive behaviours. This includes specialized morphological phenotypes such as an elongated snout with a small terminal mouth, fused jaws, absent pelvic and caudal fins, and an extended body covered with an armour of bony plates instead of scales <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#ref1> 1 ( <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html#f1> Fig. 1a). Syngnathids are also unique among vertebrates due to their ‘male pregnancy’, whereby males nourish developing embryos in a brood pouch until hatching and parturition occurs <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#ref2> 2,  <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#ref3> 3. In addition, members of the subfamily Hippocampinae (seahorses) exhibit other derived features such as the lack of a caudal fin, a characteristic prehensile tail, and a vertical body axis <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html?WT..ec_id=NATURE-20161215&spMailingID=52992218&spUserID=MjA1NTE2ODQxMAS2&spJobID=1062902411&spReportId=MTA2MjkwMjQxMQS2#ref4> 4 ( <http://www.nature.com/nature/journal/v540/n7633/full/nature20595.html#f1> Fig. 1a). To understand the genetic basis of the specialized morphology and reproductive system of seahorses, we sequenced the genome of the tiger tail seahorse, H. comes, and carried out comparative genomic analyses with the genome sequences of other ray-finned fishes (Actinopterygii).

Figure 1: Adaptations and evolutionary rate of H. comes.

 <http://www.nature.com/nature/journal/v540/n7633/fig_tab/nature20595_F1.html> Adaptations and evolutionary rate of H. comes.

a, Schematic diagram of a pregnant male seahorse. b, The phylogenetic tree generated using protein sequences. The values on the branches are the distances (number of substitutions per site) between each of the teleost fishes and the spotted gar (outgroup). Spotted gar, Lepisosteus oculatus; zebrafish, Danio rerio.

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