Cryptic diversity in Afro-tropical lowland forests: The systematics and biogeography of the avian genus Bleda

Recent investigations of distributional patterns of Afro-tropical lowland forest species have demonstrated to some degree our overall lack of understanding involving historical diversification patterns. Traditionally, researchers have relied upon two hypotheses, each of which views the lowland forest of Africa in differing roles. The Pleistocene Forest Refuge Hypothesis (PFRH) posits that biogeographic patterns of avian lowland species are explained via allopatric speciation during forest fragmentation cycles in the Pleistocene epoch (c. 1.8 Ma-11,700 Ka). The Montane Speciation Hypothesis (MSH) countered by suggesting that lowland forests are "evolutionary museums" where species, which originally evolved in montane forest refuge centers, remained without further diversification. Furthermore, investigations have largely regarded widespread, avian species which lack phenotypic variability as biogeographically "uninformative", with regards to historical biogeographic patterns. To test the tenets of these ideas, we investigated the systematics and biogeography of the genus Bleda, whose constituent species are restricted to lowland forest and are lacking in phenotypic variation. Using extracted DNA from 179 individuals, we amplified two mitochondrial genes and three nuclear loci and utilized Bayesian phylogenetic methods and molecular clock dating to develop a time-calibrated phylogeny of Bleda. We used LaGrange to develop an ancestral area reconstruction for the genus. Haplotype networks for three species were generated using Network. We recovered the four currently recognized species of Bleda, plus a monophyletic B. ugandae, a current sub-species which may warrant full species status. We found that the origins of the genus Bleda are estimated to be in the Upper Guinean forests of West Africa, dating to the Miocene (c. 7.5 Ma), while the speciation events for the rest of the genus are dated to the Pliocene (c. 5-1.8 Ma). Our analyses recovered discrete and highly differentiated geographic structuring of genetic diversity in West and Central Africa in three of five species, with many of the diversification events dating to the Pleistocene. The biogeographic patterns observed in Bleda can be explained through a combination of isolation via forest refuges during the Plio-Pleistocene and riverine barriers limiting secondary contact after forest expansion. We find evidence for the PFRH as a driver of intra-specific diversity, but conclude that it does not facilitate an explanation for speciation in the genus Bleda. The "evolutionary museum" concept furnished by the MSH is countered by our evidence of in situ diversification in the lowland forests of Africa. Additionally, our results provide strong evidence of the value of seemingly "uninformative" widespread avian taxa for revealing complex patterns of forest diversity. Overall, our study highlights that past researchers have both underestimated the amount of diversity found in lowland forests and failed to understand the complexity of historical forces shaping that diversity. Gaining a better understanding of lowland forest diversity and the historical factors which have shaped it will crucial in determining conservation tactics in the near future. (C) 2016 Elsevier Inc. All rights reserved.