Global genomics of the man-o’-war (Physalia) reveals biodiversity at the ocean surface
SH. Church, RB. Abedon & others doi: https://doi.org/10.1101/2024.07.10.602499
Abstract:
The open ocean is a vast, highly connected environment, and the organisms found there have been hypothesized to represent massive, well-mixed populations. Of these, the Portuguese man-o’-war (Physalia) is uniquely suited to dispersal, sailing the ocean surface with a muscular crest. We tested the hypothesis of a single, panmictic Physalia population by sequencing 133 genomes, and found five distinct lineages, with multiple lines of evidence showing strong reproductive isolation despite range overlap. We then scored thousands of citizen-science photos and identified four recognizable morphologies linked to these lineages. Within lineages, we detected regionally endemic subpopulations, connected by winds and currents, and identified individual long-distance dispersal events. We find that, even in these sailing species, genetic variation is highly partitioned geographically across the open ocean.
Summary:
We combined these data with an independent dataset of thousands of images of Physalia uploaded to the citizen-science website inaturalist.org, which we scored for morphological characters including sail size, tentacle arrangement, and color. From these images, we identified four recognizable morphologies, described their geographical distribution, and linked them to four of the lineages identified with genomic data. We conclude there are at least four species, three of which correspond to species proposed by scientists in the 18th and 19th centuries: P. physalis, P utriculus, and P. megalista, along with one as yet unnamed species Physalia sp. from the Tasman Sea. Within each species, we observe significant population structure, with evidence of persistent subpopulations at a regional scale, as well as evidence for individual long-distance dispersal events. Our findings indicate that, instead of one well-mixed, cosmopolitan species, there are in fact multiple Physalia species with distinct but overlapping ranges, each made up of regionally endemic subpopulations that are connected by major ocean currents and wind patterns.
Σχόλια
Some extracts from the preprint:
"Three of the morphologies we identified are congruent with species proposed by scientists centuries ago ...
.* P. physalis was named by Linneaus in 1758 based on specimens from the Atlantic that had large sails and multiple major tentacles ...
.* P. utriculus was named by Gmelin (1788), based on illustrations by La Martinière (1787) of a Pacific specimen collected on the Lapérouse expedition that had a single major tentacle, yellow-tipped gastrozooids, and a flared posterior growth zone.
.* P. megalista was named and illustrated by Lesueur and Petit (1807) from specimens from the Southern Ocean that had an short sail and a sinuously postured float.
"Each of these species was synonymized with P. physalis in later centuries; our results indicate these synonymies to have been incorrect.
"We linked these morphotypes to clusters identified through genome sequencing by analyzing the morphology of specimens we had analyzed genetically, using images taken upon collection, when available, as well as the morphology of fixed specimens ... Our results confirm that
cluster A corresponds to P. physalis,
cluster B1 to P. utriculus,
cluster C1 to P. megalista, and
cluster C2 to P. sp.
Cluster B2 could not be assigned given that given that no images of specimens were taken upon collection; ... single available fixed specimen suggested a general similarity to specimens of B1, P. utriculus
"Based on the assignment of morphotypes to clusters, we re-examined the distribution of the lineages using positively identified images. We found that
cluster A, P. physalis was observed in the N. Atlantic, consistent with genomic findings, as well as the SW. Atlantic;
cluster B1, P. utriculus was found throughout the Pacific, Indian, as well as the SW. Atlantic and Gulf of Mexico;
cluster C1, P. megalista was found in the Southern edges of the Pacific, Indian, as well as the SW. Atlantic; and
cluster C2, P. sp. was found in New Zealand, Tasmania, as well as E. Australia
"This study builds on the work and observations of sailors, swimmers, and scientists over the course of centuries. As early as the 18th century, hypotheses about multiple species emerged, based on reports from global voyages .... Among these are three of the species we observed, P. physalis, utriculus, and megalista. These species were not “cryptic”; they were proposed, debated, and ultimately rejected over the course of 250 years. Our results vindicate their original descriptions, showing clear and strong support for distinct species matching the original illustrations. The central challenge faced by taxonomists in past centuries was that there was no way to simultaneously observe live or recently beached Physalia across its huge range, and key characteristics like posture, color, and behavior are lost during fixation. These results underscore the power of participatory science and social media to provide an unprecedented lens on biodiversity.
Why not on iNat yet?
The iNat dictionary will only be updated when this paper is reviewed (this is a preprint), and it is accepted by WORMS.
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