Abstract
Seahorses have a circum-global distribution in tropical to temperate coastal waters. Yet, seahorses show many adaptations for a sedentary, cryptic lifestyle: they require specific habitats, such as seagrass, kelp or coral reefs, lack pelvic and caudal fins, and give birth to directly developed offspring without pronounced pelagic larval stage, rendering long-range dispersal by conventional means inefficient. Here we investigate seahorses’ worldwide dispersal and biogeographic patterns based on a de novo genome assembly of Hippocampus erectus as well as 358 re-sequenced genomes from 21 species. Seahorses evolved in the late Oligocene and subsequent circum-global colonization routes are identified and linked to changing dynamics in ocean currents and paleo-temporal seaway openings. Furthermore, the genetic basis of the recurring “bony spines” adaptive phenotype is linked to independent substitutions in a key developmental gene. Analyses thus suggest that rafting via ocean currents compensates for poor dispersal and rapid adaptation facilitates colonizing new habitats.
Highlights
Seahorses have a circum-global distribution in tropical to temperate coastal waters
Comprehensive studies addressing spatio-temporal diversification patterns that include dynamics of geophysical processes, as well as knowledge of the genetic bases and developmental mechanisms of key adaptive traits, are required to understand the mechanisms that drive the evolution of marine biodiversity
The radiation of seahorses (Family Syngnathidae) is a iconic and suitable model system to investigate the effects that tectonic activity and ocean current dynamics can have on the dispersal and diversification of marine taxa due to the seahorses’ dispersal by rafting[7,9], as well as to study the rapid evolution of adaptive phenotypes in new environments
Summary
The North Atlantic lineage followed north-westward oceanic currents and passed through the Tethys Sea a few million years before the initial closure of the East Tethys Seaway due to tectonic shifts about 14 Ma6,28 Consistent with this colonization route for the North Atlantic lineage a strong genetic bottleneck in their ancestral population was detected (supporting the notion that founder dispersal is common in seahorses21), a rapid population expansions was detected after crossing the Atlantic Ocean in the mid Miocene (Fig. 2a, b, Supplementary Fig. 10). About 13 Ma the ancestors of H. kelloggi and H. spinosissimus emerged as a new lineage by dispersing back into the Indo-Australian Archipelago This event may had been facilitated by a reinforced Equatorial Counter Current in the Indian Ocean after the closure of the Tethys Seaway[30], and further contributed to the high diversity in the original center of seahorse biodiversity (Fig. 2c, d).
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