Explaining rapid diversification and speciation remains a central challenge to evolutionary biology [1
]. Much work has focused on either understanding the ecology and phylogenetic history of species-rich systems that have recently diversified along ecological axes (e.g. adaptive radiations) [3
], or looking for patterns of species change in the fossil record [4
]. Taking the molecular phylogenetic/ecological approach alone, however, excludes information about extinct lineages that may substantially bias our ability to identify cases of rapid diversification [9
]. Conversely, relying on the fossil record alone limits our ability to detect evolutionary relationships between fossil taxa and some shifts in ecological function that may not be apparent from fossil character states. Ultimately, a more complete understanding of the processes that drive rapid diversification will require historical information from both molecular and fossil data. By examining systems that show recent speciation within monophyletic groups, ecological differentiation, and a strong fossil record, we can begin to link past to present processes in the understanding of the evolution of diversity.
The marine Caribbean fauna provides rare examples of diversification of monophyletic lineages within the context of well-understood changes in biogeography, oceanography, and climate. The isolation of Caribbean populations from their Indo-Pacific counterparts started ~15-17
Ma when the closure of the Tethys Sea cut off connections between the Mediterranean and Indo-Pacific [10
]. Isolation was complete ~3.45 - 4.25
Ma when the rise of the Isthmus of Panama severed all Caribbean connections to the Indo-Pacific [11
]. The period leading up to closure of the isthmus during the late Miocene to late Pliocene was characterized by changing global oceanographic circulation patterns, leading to drastic environmental, ecological, and taxonomic shifts within the Caribbean basin. Not only did the cessation of gene flow between the Pacific and Atlantic Oceans lead to widespread vicariant speciation across the newly formed isthmus [12
], but on the Caribbean side, the accompanying geological and oceanographic changes caused an overall decrease in depth, primary productivity and turbidity and an increase in salinity, temperature, and local environmental heterogeneity [11
]. Fossil records of many marine taxa during this period show elevated levels of taxonomic turnover [11
], suggesting that climatic and geological variables drove elevated rates of cladogenesis and extinction.
This taxonomic turnover is particularly striking in corals of the family Faviidae, where an examination of the stratigraphic ranges shows that all extant species originated nearly simultaneously during the Mio-Pliocene [22
]. Moreover, for faviids, this recent radiation has resulted in impressive diversification of ecological and life-history traits [23
]. Modern species of Manicina
are representative of a free-living lifestyle adapted to sediment-rich seagrass habitats that expanded during the Miocene then contracted during the Plio-Pleistocene [15
]. In contrast, species of the brain coral genus Diploria
tend to be reef-builders, dominating shallow water reef platforms in Pleistocene and modern times [25
]. These two “sediment” and “reef” clades appear to share a common ancestor and ecological diversification seems to have occurred over a short period of geological time, suggesting it is tied to the contemporaneous increase in environmental heterogeneity [29
]. Yet this punctuated diversification event is inferred from a fossil record, which may be incomplete or contain uncertainties in dating and taxonomic relationships that may influence our interpretation of past patterns.
Molecular data combined with well sampled fossil records provide opportunities to test existing evolutionary hypotheses and extend our understanding of both the tempo and mode of evolutionary diversification. In the Scleractinia, deep divergences between coral orders, suborders and families are increasingly well understood [30
]. Yet a recent series of phylogenies exploring relationships at the familial level and below have demonstrated pervasive polyphyly and paraphyly at the generic level [34
]. In addition, these studies have shown that between ocean basins, species group geographically rather than taxonomically [35
]. In particular, Atlantic lineages of Faviidae and Mussidae appear to be more closely related to other Atlantic lineages than to congeners or even confamilials in other ocean basins. This geographic split supports the evidence from the fossil record of a radiation of the Caribbean coral fauna before complete isolation from the Pacific. However, the failure to resolve species relationships within the traditional coral family Faviidae, and a long history of taxonomic difficulties in identifying and classifying corals [32
] demands an independent assessment of trends apparent in the fossil record.
To explore the tempo and mode of this evolutionary diversification, we unite a new multi-locus phylogeny of the Caribbean Faviidae with new stratigraphic compilations from the fossil record. Our well-sampled phylogeny allows Bayesian approaches to place these relationships into a temporal context by dating divergence times based on molecular data and fossil calibrations. We compare our time-calibrated phylogeny to temporal patterns of origination and extinction revealed by the Neogene fossil record, and find remarkable congruence between data sets. The timing of events revealed by this analysis strongly implicates paleoenvironmental changes as drivers of diversification in scleractinian corals.