A multi-locus inference of the evolutionary diversification of extant flamingos (Phoenicopteridae)

Abstract

BackgroundModern flamingos (Phoenicopteridae) occupy a highly specialized ecology unique among birds and represent a potentially powerful model system for informing the mechanisms by which a lineage of birds adapts and radiates. However, despite a rich fossil record and well-studied feeding morphology, molecular investigations of the evolutionary progression among modern flamingos have been limited. Here, using three mitochondrial (mtDNA) markers, we present the first DNA sequence-based study of population genetic variation in the widely distributed Chilean Flamingo and, using two mtDNA and 10 nuclear (nDNA) markers, recover the species tree and divergence time estimates for the six extant species of flamingos. Phylogenetic analyses include likelihood and Bayesian frameworks and account for potential gene tree discordance. Analyses of divergence times are fossil calibrated at the divergence of Mirandornithes (flamingos + grebes) and the divergence of crown grebes.ResultsmtDNA sequences confirmed the presence of a single metapopulation represented by two minimally varying mtDNA barcodes in Chilean flamingos. Likelihood and Bayesian methods recovered identical phylogenies with flamingos falling into shallow-keeled (comprising the Greater, American and Chilean Flamingos) and deep-keeled (comprising the Lesser, Andean and James’s Flamingos) sub-clades. The initial divergence among flamingos occurred at or shortly after the Mio-Pliocene boundary (6–3 Ma) followed by quick consecutive divergences throughout the Plio-Pleistocene. There is significant incongruence between the ages recovered by the mtDNA and nDNA datasets, likely due to mutational saturation occurring in the mtDNA loci.ConclusionThe finding of a single metapopulation in the widespread Chilean Flamingo confirms similar findings in other widespread flamingo species. The robust species phylogeny is congruent with previous classifications of flamingos based on feeding morphology. Modern phoenicopterids likely originated in the New World with each sub-clade dispersing across the Atlantic at least once. Our divergence time estimates place flamingos among the youngest families of birds, counter to the classical notion of flamingos as among the oldest based on biogeography and the fossil record. Finally, we designate ‘Phoeniconaias’ as a junior synonym of ‘Phoenicoparrus’ and redefine the latter genus as containing all flamingos more closely related to Phoenicoparrus andinus than Phoenicopterus roseus.

Evidence of gene orthology and trans‐species polymorphism, but not of parallel evolution, despite high levels of concerted evolution in the major histocompatibility complex of flamingo species

“…Bayesian phylogenetic reconstruction of MHC sequences in flamingo species is therefore consistent with high rates of concerted evolution disrupting divergence of orthologs. We are nonetheless confident that MHC Class IIB duplication occurred prior to flamingo speciation around 3–6 million years ago (Torres et al ., ), based on the following lines of evidence. First, we found the same number of gene duplications of MHC Class IIB across all six extant flamingo species.…”

“…The latter therefore implies that there should be similar pathogen‐mediated selection pressure between sympatric flamingo species. An important beneficial feature of the flamingo model in respect to the understanding of MHC evolution is that the phylogeny of the flamingo species does not match with their cross‐Atlantic geographical distribution (Torres et al ., ; Fig. ).…”

“…Cladogram showing the relationships of the extant flamingo species adapted from Torres et al . () (copyright pending) and the approximate geographical distribution of each flamingo species. The flamingos fall out in two subclades with high support, which is not congruent with their geographic distribution.…”

Opposing demographic histories reveal rapid evolution in grebes (Aves: Podicipedidae)

“…To estimate divergence times for the entire eared grebe clade based on the protein-coding mtDNA loci, constraints were used based on node age estimates from a dataset including samples of all grebe genera (Ogawa et al 2008). Fossil constraints on this larger dataset included the earliest known crown (modern) grebe Thiornis sociata (8.7 myr, 65 myr; Ksepka et al 2013) and the earliest known stem flamingo Paleolodus (31 myr, 65 myr; van Tuinen et al 2001, Ericson et al 2006, Torres et al 2014, which provided age range estimates for nodes in this study's analysis. Both of these fossil lineages correspond to recommended (Parham et al 2012) justifications for fossil calibration, while the slightly older Early Miocene Miobaptus and Late Oligocene grebe material from Kazakhstan (Kurochkin 1976) remains either formally undescribed or an uncertain member of crown Podicipedidae (Ksepka et al 2013).…”

Shared evolutionary origin of major histocompatibility complex polymorphism in sympatric lemurs

“…This pattern echoes previous observations in two stickleback species that diverged at least 7 million years ago (Mya) (Bell & Foster, ; Lenz et al., ) and six flamingo species that diverged ca. 3–6 Mya (Torres, Ogawa, Gillingham, Ferrari, & Van Tuinen, ; Gillingham et al., ). Moreover, co‐ancestry scores for DRB were significantly correlated with phylogenetic distances among species, suggesting that functionally similar alleles are progressively lost as species diverge.…”