Jessica R. Eberhard

A Multilocus Molecular Phylogeny of the Parrots (Psittaciformes): Support for a Gondwanan Origin during the Cretaceous

The question of when modern birds (Neornithes) first diversified has generated much debate among avian systematists. Fossil evidence generally supports a Tertiary diversification, whereas estimates based on molecular dating favor an earlier diversification in the Cretaceous period. In this study, we used an alternate approach, the inference of historical biogeographic patterns, to test the hypothesis that the initial radiation of the Order Psittaciformes (the parrots and cockatoos) originated on the Gondwana supercontinent during the Cretaceous. We utilized broad taxonomic sampling (representatives of 69 of the 82 extant genera and 8 outgroup taxa) and multilocus molecular character sampling (3,941 bp from mitochondrial DNA (mtDNA) genes cytochrome oxidase I and NADH dehydrogenase 2 and nuclear introns of rhodopsin intron 1, tropomyosin alpha-subunit intron 5, and transforming growth factor ss-2) to generate phylogenetic hypotheses for the Psittaciformes. Analyses of the combined character partitions using maximum parsimony, maximum likelihood, and Bayesian criteria produced well-resolved and topologically similar trees in which the New Zealand taxa Strigops and Nestor (Psittacidae) were sister to all other psittaciforms and the cockatoo clade (Cacatuidae) was sister to a clade containing all remaining parrots (Psittacidae). Within this large clade of Psittacidae, some traditionally recognized tribes and subfamilies were monophyletic (e.g., Arini, Psittacini, and Loriinae), whereas several others were polyphyletic (e.g., Cyclopsittacini, Platycercini, Psittaculini, and Psittacinae). Ancestral area reconstructions using our Bayesian phylogenetic hypothesis and current distributions of genera supported the hypothesis of an Australasian origin for the Psittaciformes. Separate analyses of the timing of parrot diversification constructed with both Bayesian relaxed-clock and penalized likelihood approaches showed better agreement between geologic and diversification events in the chronograms based on a Cretaceous dating of the basal split within parrots than the chronograms based on a Tertiary dating of this split, although these data are more equivocal. Taken together, our results support a Cretaceous origin of Psittaciformes in Gondwana after the separation of Africa and the India/Madagascar block with subsequent diversification through both vicariance and dispersal. These well-resolved molecular phylogenies will be of value for comparative studies of behavior, ecology, and life history in parrots.

Behavioral flexibility and species invasions: the adaptive flexibility hypothesis

Behavioral flexibility is an important adaptive response to changing environments for many animal species. Such plasticity may also promote the invasion of novel habitats by introduced species by providing them with the ability to expand or change their ecological niche, a longstanding idea with recent empirical support. At the individual level, flexibility may arise through innovation, in which an individual invents a new behavior, or through social learning, in which an individual adopts a behavior used by others. There is increasing evidence that the adaptive value of these two modes of learning, and the overall expression of behavioral flexibility, may vary with social and environmental context. In this paper, we propose that invasive species may change the degree to which they express behavioral flexibility in an adaptive manner during the different stages of invasion. Specifically, the “adaptive flexibility hypothesis” predicts that the expression of behavioral flexibility, and thus the diversity of behaviors observed in a population, will be high during the initial stage of introduction into a novel environment due to innovation, followed by a decline in behavioral diversity during the establishment and growth of a founding population due to social learning of successful behavioral variants. We discuss several alternatives to this hypothesis and suggest empirical and theoretical tests of these hypotheses. This “adaptive flexibility hypothesis” suggests that a more nuanced approach to the study of the behaviors employed by individuals in populations at different invasion stages could generate new insight into the importance of such flexibility during species invasions, and the evolution of behavioral plasticity in general

PHYLOGENY AND BIOGEOGRAPHY OF THE AMAZONA OCHROCEPHALA (AVES: PSITTACIDAE) COMPLEX

Abstract We present a phylogenetic analysis of relationships among members of the Amazona ochrocephala species complex of parrots, a broadly distributed group in Middle and South America that has been a “taxonomic headache.” Mitochondrial DNA sequence data are used to infer phylogenetic relationships among most of the named subspecies in the complex. Sequence-based phylogenies show that Middle American subspecies included in the analysis are reciprocally monophyletic, but subspecies described for South America do not reflect patterns of genetic variation. Samples from the lower Amazon cluster with samples collected in western Amazonia—not with samples from Colombia and Venezuela, as was predicted by subspecies classification. All subspecies of the complex are more closely related to one another than to other Amazona species, and division of the complex into three species (A. ochrocephala, A. auropalliata, and A. oratrix) is not supported by our data. Divergence-date estimates suggest that these parrots arrived in Middle America after the Panama land-bridge formed, and then expanded and diversified rapidly. As in Middle America, diversification of the group in South America occurred during the Pleistocene, possibly driven by changes in distribution of forest habitat.

Genetic evidence for high propagule pressure and long-distance dispersal in monk parakeet (Myiopsitta monachus) invasive populations

The monk parakeet (Myiopsitta monachus) is a successful invasive species that does not exhibit life history traits typically associated with colonizing species (e.g., high reproductive rate or long‐distance dispersal capacity). To investigate this apparent paradox, we examined individual and population genetic patterns of microsatellite loci at one native and two invasive sites. More specifically, we aimed at evaluating the role of propagule pressure, sexual monogamy and long‐distance dispersal in monk parakeet invasion success. Our results indicate little loss of genetic variation at invasive sites relative to the native site. We also found strong evidence for sexual monogamy from patterns of relatedness within sites, and no definite cases of extra‐pair paternity in either the native site sample or the examined invasive site. Taken together, these patterns directly and indirectly suggest that high propagule pressure has contributed to monk parakeet invasion success. In addition, we found evidence for frequent long‐distance dispersal at an invasive site (∼100 km) that sharply contrasted with previous estimates of smaller dispersal distance made in the native range (∼2 km), suggesting long‐range dispersal also contributes to the species’ spread within the United States. Overall, these results add to a growing body of literature pointing to the important role of propagule pressure in determining, and thus predicting, invasion success, especially for species whose life history traits are not typically associated with invasiveness.

Rearrangement and evolution of mitochondrial genomes in parrots

Mitochondrial genome rearrangements that result in control region duplication have been described for a variety of birds, but the mechanisms leading to their appearance and maintenance remain unclear, and their effect on sequence evolution has not been explored. A recent survey of mitochondrial genomes in the Psittaciformes (parrots) found that control region duplications have arisen independently at least six times across the order. We analyzed complete mitochondrial genome sequences from 20 parrot species, including representatives of each lineage with control region duplications, to document the gene order changes and to examine effects of genome rearrangements on patterns of sequence evolution. The gene order previously reported for Amazona parrots was found for four of the six independently derived genome rearrangements, and a previously undescribed gene order was found in Prioniturus luconensis, representing a fifth clade with rearranged genomes; the gene order resulting from the remaining rearrangement event could not be confirmed. In all rearranged genomes, two copies of the control region are present and are very similar at the sequence level, while duplicates of the other genes involved in the rearrangement show signs of degeneration or have been lost altogether. We compared rates of sequence evolution in genomes with and without control region duplications and did not find a consistent acceleration or deceleration associated with the duplications. This could be due to the fact that most of the genome rearrangement events in parrots are ancient, and additionally, to an effect of body size on evolutionary rate that we found for mitochondrial but not nuclear sequences. Base composition analyses found that relative to other birds, parrots have unusually strong compositional asymmetry (AT- and GC-skew) in their coding sequences, especially at fourfold degenerate sites. Furthermore, we found higher AT skew in species with control region duplications. One potential cause for this compositional asymmetry is that parrots have unusually slow mtDNA replication. If this is the case, then any replicative advantage provided by having a second control region could result in selection for maintenance of both control regions once duplicated.

Phylogeography of the Military Macaw (Ara militaris) and the Great Green Macaw (A. Ambiguus) Based on MTDNA Sequence Data

ABSTRACT The Military Macaw (Ara militaris) and the Great Green Macaw (A. ambiguus) are species whose close relationship is reflected in their morphological similarity as well as their geographic ranges. Military Macaws have a disjunct distribution, found in Mexico as well as several areas in South America, while Great Green Macaws have two or more disjunct populations from Honduras to eastern Ecuador. We used mitochondrial sequence data to examine the phylogenetic relationships between these two species, and also among representative samples across their ranges. Our data clearly support recognition of the two species as being distinct evolutionary lineages, and while we found significant phylogeographic structure within A. militaris (between samples collected in eastern and western Mexico), we did not find any evidence of lineage divergence between A. ambiguus from Costa Rica and Ecuador.