Why are so few island bryophytes endemic?

Endemism, a hallmark of island biodiversity, reaches its lowest levels among bryophytes compared with other land plants. Whether this pattern reflects low diversification rates, and why, or whether it is a result of loss of endemicity due to extinctions or subsequent continental (back-)colonization, is examined here through a review of available evidence in the Macaronesian flora. Significant genetic differentiation (G_ST, based on allele frequencies) was consistently found between Macaronesian and continental populations, ruling out the hypothesis that intense migrations necessarily hamper differentiation. A significant phylogeographical signal in the data (N_ST > G_ST; where N_ST is a G_ST analog incorporating phylogenetic relationships among alleles), involving higher mutation rates than dispersal rates and evidencing incipient speciation, was further found in more than 1/3 of the species investigated. The significantly higher average N_ST between extra-European regions and Macaronesia compared to Europe and Macaronesia suggests, however, that incipient speciation is more likely to occur between distant (Macaronesian versus extra-European) than closer (Macaronesian versus European) populations. In line with this, ancestral area estimations in Macaronesian endemic bryophyte species revealed that at least 50% of them have an extra-European origin, in contrast with the almost exclusively (>90%) European/Mediterranean origin of Macaronesian endemic spermatophytes. Allopatric speciation via long-distance dispersal and subsequent divergence of a single endemic species prevails in island bryophytes, wherein sympatric radiations virtually never occur. Such a speciation mode does not trigger high rates of endemism, in contrast to radiations in Macaronesian spermatophytes, which contribute to 56% of the total number of endemics. Several mechanisms may explain the failure of island bryophytes to diversify in situ, including the fact that oceanic islands are too small or insufficiently isolated from each other or from continents to promote sympatric speciation, the lack of key innovations, and phylogenetic niche conservatism for stable habitats not prone to trigger radiations. In comparison with spermatophytes, continental (back-)colonization further largely prevails in bryophytes and, unlike in many instances in angiosperms, is not followed by in situ speciation on the mainland. The consequent loss of the endemic status of species that did speciate on islands but subsequently enlarged their range further accounts for the low rates of endemism among island bryophyte floras and invalidates the use of endemism rates as a proxy of speciation rates in this group.