Subspecies designation is widely used to describe taxa below species but above geographical populations. What patterns of genomic variation is expected if taxa are designated as subspecies? In this study, we carry out such a survey on the mangrove tree Avicennia marina of the Indo-West Pacific coasts. This species has three subspecies, distinguished by morphological traits and geographical distribution. We collected samples from 16 populations (577 individuals) covering all three subspecies and sequenced 94 nuclear genes. We reveal comprehensive genetic divergence among subspecies, generally higher than among geographical populations within subspecies. The level of genetic diversity differs among the three subspecies, possibly hinting at a degree of separation among their gene pools. We observed that divergence varies from locus to locus across the genome. A small portion of the genome is most informative about subspecies delineation while the rest is undifferentiated or slightly differentiated, hinting at uneven gene flow and incomplete isolation. The three subspecies likely split simultaneously with gene flow among lineages. This reticulate evolution results in some discordance between morphology and genetics in areas of population contact. In short, A. marina subspecies show species-like patterns in some respects and population-like patterns in others. This “ambiguity” is expected at a stage between structured populations and full species, thus the observed patterns strengthen the subspecies designation. We propose that subspecies designation is informative in predicting genomic landscape of divergences and useful in making conservation decisions.

The designation of subspecies has often been uncertain in systematics. In addition to phenotypic divergence, designation of subspecies may need to be supplemented by population genetic analyses. In this study, we perform such a survey of the mangrove tree Avicennia marina on Indo-West Pacific coasts. This species harbors three morphological groups. We collected samples from 16 populations (577 individuals) and sequenced 94 nuclear genes. Three genetic features support the subspecies designation for the three morphological subgroups. First, the observed genetic divergence is concordant with the morphological differences, with discordance found in zones of coexistence. Second, the three groups differ in the level of genetic diversity as well as in the demographic history, suggesting a degree of ecological differentiation. Third, and most important, the divergence level varies from locus to locus across the genome. A small portion of the genome is most informative about subspecies delineation, thus hinting the uneven exchange of genes. Such locus-dependent gene flow is expected for incompletely isolated groups. This last point suggests that the reduction in gene flow can be observed at some loci, thus hinting incipient reproductive isolation. In short, the three groups of A. marina appear to have evolved far beyond the stage of structured populations, but not to the point of full species. Hence, the subspecies designation is warranted. We believe these considerations can be generalized to other taxa.

The designation of subspecies has long been controversial in systematics. In addition to phenotypic divergence, subspecies designation may need to incorporate population genetic analyses. In this study, we perform such a survey on three subspecies of the mangrove tree Avicennia marina, distributed along the Indo-West Pacific coasts. Samples from 16 populations (577 individuals) were collected and 94 nuclear genes were sequenced. We identify four genetic features that support the subspecies designation in this genus. First, genetic divergence that delineates the three subspecies is evident, with discordance found mainly in zones of secondary contact. Moreover, levels of genetic diversity within local populations differ among subspecies. Second, the three subspecies have separate demographic histories inferred by computational modeling. Third, gene flow is detected between subspecies indicating little or no reproductive isolation. Fourth, the delineation of the subspecies varies from locus to locus across the genome, thus hinting continual but uneven exchanges of genes. All these features indicate that the three taxa have proceeded far beyond structured populations. Since they have not satisfied the criteria for full-species designation, the subspecies designation is warranted. We believe these considerations can be generalized to other taxa.