Molecular Phylogeny and Evolution of Amazon Parrots in the Greater Antilles

Abstract

Amazon parrots (Amazona spp.) colonized the islands of the Greater Antilles from the Central American mainland, but there has not been a consensus as to how and when this happened. Today, most of the five remaining island species are listed as endangered, threatened, or vulnerable as a consequence of human activity. We sequenced and annotated full mitochondrial genomes of all the extant Amazon parrot species from the Greater Antillean (A. leucocephala (Cuba), A. agilis, A. collaria (both from Jamaica), A. ventralis (Hispaniola), and A. vittata (Puerto Rico)), A. albifrons from mainland Central America, and A. rhodocorytha from the Atlantic Forest in Brazil. The assembled and annotated mitogenome maps provide information on sequence organization, variation, population diversity, and evolutionary history for the Caribbean species including the critically endangered A. vittata. Despite the larger number of available samples from the Puerto Rican Parrot Recovery Program, the sequence diversity of the A. vittata population in Puerto Rico was the lowest among all parrot species analyzed. Our data support the stepping-stone dispersal and speciation hypothesis that has started approximately 3.47 MYA when the ancestral population arrived from mainland Central America and led to diversification across the Greater Antilles, ultimately reaching the island of Puerto Rico 0.67 MYA. The results are presented and discussed in light of the geological history of the Caribbean and in the context of recent parrot evolution, island biogeography, and conservation. This analysis contributes to understating evolutionary history and empowers subsequent assessments of sequence variation and helps design future conservation efforts in the Caribbean.

Changes in parrot diversity after human arrival to the Caribbean

“…See SI Appendix , Tables S3 and Table S5 for extended data. These data were combined with mitochondrial genome data generated from our efforts, Kolchanova et al ( 40 ), and from mitochondrial bycatch from samples produced by Smith et al ( 41 ) and Olekysyk et al ( 42 ) to produce a mitochondrial genome phylogeny. Raw data for each of these ancient samples are available on NCBI SRA (PRJNA913959) ( 38 ), and annotated mitochondrial genome data are accessioned on NCBI GenBank.…”

“…The UCE dataset recovered a topology for Greater Antillean Amazona that was consistent with previous studies in that these species were a monophyletic group (refs. 40 – 41 , 46 and SI Appendix , Fig. S1 ).…”

Genomics of Adaptation and Speciation

“…Answering questions about speciation, adaptation, and extinction does not require the newest and most advanced sequencing technologies, and limited sets of data can be used. The examples in this issue included studies of large structural and chromosomal variation [ 9 , 13 ] (Beklemisheva et al, 2020; Galindo et al, 2021), mtDNA and/or limited nuclear marker approaches to phylogenetics [ 24 ] (Kolchanova et al, 2021), hybridogenesis [ 10 ] (Miura et al, 2021), comparative transcriptomics [ 14 ] (Zhao and Kishino, 2020), and genome-wide studies of SNP variation using a combination of low-coverage sequencing and genotyping [ 15 , 16 ] (de La Torre et al, 2021; Mahtani-Williams et al, 2020). However, newer, more contiguous assemblies may allow for a better estimation of the genetic diversity, localization, and visualization of the distribution of genome diversity in the evolutionary context of adaptation and speciation [ 21 ] (Totikov et al, 2021).…”

“…Genome data were used to investigate times of speciation in the context of the island colonization of the Greater Antilles by a group of Amazon parrots [11,12] (Kolchanova et al, 2021(Kolchanova et al, , 2019. A collection of parrot genomes was aligned to reconstruct phylogenetic relationships and estimate the times of speciation, providing several hypotheses based on a combination of molecular data and biogeographic modeling to understand the history of speciation of the parrots from the Caribbean islands.…”

“…(Beklemisheva et al, 2020;Galindo et al, 2021), mtDNA and/or limited nuclear marker approaches to phylogenetics[24] (Kolchanova et al, 2021), hybridogenesis[10] (Miura et al, 2021), comparative transcriptomics[14] (Zhao and Kishino, 2020), and genome-wide studies of SNP variation using a combination of low-coverage sequencing and genotyping[15,16] (de La Torre et al, 2021; Mahtani-Williams et al, 2020).…”