Global genomics of the man-o'-war (Physalia) reveal biodiversity at the ocean surface

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. SummaryThe open ocean is a vast and highly connected environment. The organisms that live there have a significant capacity for dispersal and few geographic boundaries to separate populations. Of these, the Portuguese man-o-war or bluebottle (genus Physalia) is uniquely suited to long-distance travel, using its gas-filled float and muscular crest to catch the wind and sail the sea surface. Physalia are distributed across the globe, and like many pelagic organisms, have been hypothesized to represent a massive, well-mixed population that extends across ocean basins. We tested this hypothesis by sequencing whole genomes of 133 samples collected from waters of over a dozen countries around the globe. Our results revealed five distinct lineages, with multiple lines of evidence indicating strong reproductive isolation, despite regions of range overlap. 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.