Genomics-Based Phylogenetic and Population Genetic Analysis of Global Samples Confirms Halophila johnsonii Eiseman as Halophila ovalis (R.Br.) Hook.f.

Michelle Waycott,Eric Bricker,Ainsley Calladine,Ed Biffin,Kor-Jent Van Dijk

doi:10.3389/fmars.2021.740958

Michelle Waycott, Eric Bricker + Show 3 more

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https://doi.org/10.3389/fmars.2021.740958

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Abstract

Halophila johnsonii is an endangered seagrass species that is restricted to the southeast coast of Florida, United States. Its taxonomic status has been called into question, in particular, given the close morphological and genetic similarity of H. johnsonii and the widely distributed and morphologically variable Halophila ovalis, which is largely restricted to the Indo-Pacific region. While a close relationship to H. ovalis is uncontroversial, it remains uncertain whether H. johnsonii represents a distinct lineage or is a recent introduction to the Florida region. Given the conservation status of H. johnsonii, distinguishing these alternatives has important implications for the management of the species and its habitat. Here, we develop molecular data sets for samples of H. johnsonii and H. ovalis including DNA sequences, genome-wide SNPs and microsatellites with the view to resolving the affinities of H. johnsonii with respect to the wider H. ovalis complex. Phylogenetic hypotheses based upon plastid (∼18000 bp) and low copy nuclear DNA (∼6500 bp) sequences derived from hybrid capture, along with 990 genome-wide ddRAD SNPs consistently resolved H. johnsonii within H. ovalis. Specifically, we found a close affinity between H. johnsonii and H. ovalis sampled from the east coast of Africa. In addition, Halophila specimens collected in Antigua, which are within the range of morphological variation typical for H. ovalis, are virtually identical to H. johnsonii and the East African H. ovalis samples based upon DNA sequence analyses and these group together using Bayesian clustering analyses of microsatellites and ddRAD SNPs. We conducted population genetic analyses using large number of H. johnsonii samples collected over a 17-year period. Genotypic data generated through microsatellites and ddRAD SNPs revealed genetic uniformity for all 132 H. johnsonii samples across the Indian River Lagoon, Florida, while samples of H. ovalis from Antigua shared the same genotype as H. johnsonii. We conclude that the lack of genetic diversity and the absence of sexual reproduction strongly indicates that the total range of H. johnsonii is actually one clone that is closely related to populations in Africa and Antigua and may be derived from a recent introduction from one of those regions.

Highlights

Halophila johnsonii Eisman is a shallow water marine angiosperm, or seagrass, which has a restricted distribution in areas of the southeast coast of Florida (Virnstein et al, 2009)
A large sample set was screened with ten microsatellite loci and a smaller sample was tested with the 990 SNP loci that were generated through ddRAD
H. johnsonii is listed under the United States Fish and Wildlife Service ESA and its taxonomic status is of interest to many stakeholders as changes could have farreaching implications for the ongoing management of the species and its habitat

Summary

Introduction

Halophila johnsonii Eisman is a shallow water marine angiosperm, or seagrass, which has a restricted distribution in areas of the southeast coast of Florida (Virnstein et al, 2009). H. johnsonii was first noted along the east coast of Florida in the latter half of the last century (Phillips, 1960) and was subsequently described as a new species (Eiseman and McMillan, 1980). It is differentiated from other Halophila Thouars species found in the Atlantic by its smooth leaf margins on leaf-pairs at each node and leaf blades lacking both serrations and hairs. As a relatively recently described species, and a seagrass endemic to the east coast of Florida, early collections of H. johnsonii may have been referred to Halophila decipiens Ostenf. As a relatively recently described species, and a seagrass endemic to the east coast of Florida, early collections of H. johnsonii may have been referred to Halophila decipiens Ostenf. or H. baillonii Asch. (e.g., Figure 46 in Phillips, 1960)

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