Speciation with gene flow on Lord Howe Island

Abstract

Understanding the processes underlying the origin of species is a fundamental goal of biology. It is widely accepted that speciation requires an interruption of gene flow between populations: ongoing gene exchange is considered a major hindrance to population divergence and, ultimately, to the evolution of new species. Where a geographic barrier to reproductive isolation is lacking, a biological mechanism for speciation is required to counterbalance the homogenizing effect of gene flow. Speciation with initially strong gene flow is thought to be extremely rare, and few convincing empirical examples have been published. However, using phylogenetic, karyological, and ecological data for the flora of a minute oceanic island (Lord Howe Island, LHI), we demonstrate that speciation with gene flow may, in fact, be frequent in some instances and could account for one in five of the endemic plant species of LHI. We present 11 potential instances of species divergence with gene flow, including an in situ radiation of five species of Coprosma (Rubiaceae, the coffee family). These results, together with the speciation of Howea palms on LHI, challenge current views on the origin of species diversity.Metrosideros | sympatric speciation | geography of speciation S peciation with strong gene flow is controversial among evolutionary biologists (1-3). Unlike speciation without gene flow (e.g., allopatric speciation and polyploid speciation) (4), it requires both divergent natural selection and a mechanism to promote nonrandom mating (5-7). Theoretically, these conditions might coincide via a pleiotropic magic trait, through linkage disequilibrium between genes involved in local adaptation and assortative mating, or because habitat differences within a species' range produce divergent genetic adaptations as well as plastic responses that confer reproductive isolation (e.g., environmentally controlled shifts in flowering time) (3,5,(7)(8)(9)(10). The most controversial incarnation of speciation occurs in sympatry, when gene exchange is high. Numerous definitions of sympatric speciation have been proposed since it was first outlined by Charles Darwin (11). Population genetic definitions focus on random mating with respect to location or habitat of the mating partners. For the biogeographic definition, which we adopt here, the absence of geographic isolation is the key criterion. The relative merits and disadvantages of both views continue to be debated (1-3, 7, 8, 12, 13).In plants, evidence for the influence of sympatric speciation with strong gene flow remains sparse, with a single study on the Howea palms of Lord Howe Island (LHI) presenting the only conclusive evidence (14, 15). On the other hand, sympatric speciation via polyploidization is well known in plants and is thought to have contributed significantly to species diversity but is not thought to involve ongoing gene flow (16). Very few studies have attempted to quantify the frequency of speciation without geographic isolation, and those that have indicate that it is excep...

Incipient radiation within the dominant Hawaiian tree Metrosideros polymorpha

“…Metrosideros operculata is a rupicolous shrub endemic to New Caledonia (Dawson, 1992) and is nested within a local radiation of the subgenus Mearnsia (Wright et al, 2000). Metrosideros sclerocarpa (Dawson in Green, 1990) is a species endemic to Lord Howe island that likely evolved in situ (Papadopulos et al, 2011) and is most commonly found near creeks. This species belongs to the subgenus Metrosideros, which also contains the Hawaiian species.…”

Speciation in a small space

“…Biogeographic work on birds and lizards has failed to turn up a single case of sister species on small islands (9, 10); similar conclusions come from a recent survey of several animal and plant groups (11). In response, Papadopulos et al (1) suggest that "speciation in the face of strong gene flow may be a botanical specialty. "…”

“…By including genera in which molecular phylogenies involve a smaller percentage of the congeneric species (16-54%), Papadopulos et al (1) find nine more species that may have resulted from sympatric splits on LHI: two species in the genus Alyxia, two in Geniostoma, and two and three species, respectively, in the fern genera Grammitis and Asplenium. These cases, however, are more doubtful: incomplete phylogenies may miss some true sister species that live in other places, invalidating some examples of sympatric speciation.…”

“…Papadopulos et al (1), however, use a method designed to increase the likelihood of identifying such cases: one simply surveys species in areas, like isolated oceanic islands and tiny lakes, where the geographic isolation of populations was always unlikely. If one finds endemic sister species in such places, then they probably formed there (3).…”

Contemporary and future studies in plant speciation, morphological/floral evolution and polyploidy: honouring the scientific contributions of Leslie D. Gottlieb to plant evolutionary biology

“…Data from molecular markers and ecological studies show the potential for selection to drive divergence in the face of gene flow and recombination [37][38][39][40][41]. In his studies of Stephanomeria, Gottlieb was concerned with how initial divergence could have occurred and how the rarer derivative species could coexist with its progenitor at the same locality.…”