Frank E. Rheindt

Genetic Introgression: An Integral but Neglected Component of Speciation in Birds

The Auk, Vol. 128, Number 4, pages 620−632. ISSN 0004-8038, electronic ISSN 1938-4254.  2011 by The American Ornithologists’ Union. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals. com/reprintInfo.asp. DOI: 10.1525/auk.2011.128.4.620 3E-mail: frankrheindt@yahoo.com.au Hybridization, or the act of reproduction between different species, is common in birds (Grant and Grant 1992) and can be an agent of adaptive evolution (Veen et al. 2001). When hybridization occurs, a species’ genetic material may enter the gene pool of another and thereby introduce genetic novelty. This process is called “genetic introgression” (hereafter “introgression”; Anderson 1949). Although known for decades, the incidence of introgression in nature has long been underappreciated (e.g., Currat et al. 2008). Only recently have evolutionists come to regard it as an important and pervasive mechanism in speciation, in the maintenance of genetic diversity and in the introduction of advantageous novelty into the gene pool (Arnold et al. 1999, Noor et al. 2000, Seehausen 2004). In fact, genetic data now suggest that our own species may have undergone a complicated history of introgression with at least two extinct hominine lineages (Green et al. 2010, Reich et al. 2010). Another reason why introgression is an important topic is the impact of human-induced climate change, which is rapidly shifting vegetation boundaries and creating new hybrid zones, with little-known consequences for the genetic integrity of species (Mank et al. 2004, Brumfield 2010). There has been a tremendous increase in introgressionrelated avian research since a comprehensive overview of the introgression complex between the Blue-winged Warbler (Vermivora cyanoptera) and the Golden-winged Warbler (V. chrysoptera) appeared in The Auk five years ago (Confer 2006). Here, we seek to fill a gap by summarizing the most important recent advances in avian introgression research and our current understanding of locus-specific differences in introgression dynamics, the detection of introgression, its directionality, and its relevance to conservation, phylogenetics, and speciation research.

The impact of roads on birds: Does song frequency play a role in determining susceptibility to noise pollution?@@@Die Auswirkungen von Straßen auf Vögel: Ist Gesangsfrequenz ein Faktor für Lärmempfindlichkeit?

Traffic noise is known to have a negative impact on bird populations in general, but little is known about the mechanisms by which sound pollution affects bird communities. However, a knowledge of these mechanisms is imperative if we want to account for the differences in susceptibility to traffic noise that exist between species, and may thus be critical for conservation action. To address this issue, population assessments were carried out in a contiguous area of oak-beech forest at differing distances from a much frequented motorway to determine the road effect on the whole bird community. As expected, species richness and diversity decreased towards the motorway, and bird abundance was significantly lower along the motorway than in the control area. However, a few species defied the negative impact of the motorway. The songs of the more abundant passerines were analysed with regard to three frequency parameters to determine whether or not a relationship exists between the song pitch of a species and its sensitivity to noise pollution. A significant relationship was found between dominant frequency and decline in abundance towards the motorway, which indicates that having a higher-pitched song with frequencies well above those of traffic noise makes a bird less susceptible to noise pollution. These results suggest that acoustic masking is one of the mechanisms by which traffic noise negatively affects passerine density along roads. Verkehrslärm hat negative Auswirkungen auf Vogelbestände. Sehr wenig ist jedoch bekannt über die Mechanismen, durch welche Lärm zur Beeinträchtigung von Vogelgemeinschaften beiträgt. Dabei ist die Kenntnis eben dieser Mechanismen unerlässlich, wenn man Vorhersagen treffen will bezüglich der Unterschiede in Lärmempfindlichkeit, die es zwischen verschiedenen Arten gibt, beispielsweise im Rahmen von Schutzprogrammen. Um dieser Frage nachzugehen, wurden Bestandserfassungen in einem zusammenhängenden Eichen-Buchenwaldgebiet in unterschiedlichen Abständen zu einer viel befahrenen Autobahn durchgeführt. So konnten die Auswirkungen der Straße auf die gesamte Vogelgemeinschaft erfasst werden. Erwartungsgemäß nahmen Artenreichtum und Diversität zur Autobahn hin ab. Ebenso waren Vogelabundanzen entlang der Autobahn signifikant tiefer als im Kontrollgebiet. Dennoch zeigten sich einige Arten nicht beeinträchtigt durch die Autobahn. Um festzustellen, ob zwischen Gesangsfrequenz und Lärmempfindlichkeit ein Zusammenhang besteht, wurden die Gesänge der häufigeren Singvogelarten in Bezug auf drei Frequenzparameter untersucht. Die dominante Frequenz eines Gesanges korrelierte dabei signifikant mit der Bestandsabnahme zur Autobahn hin, was andeutet, dass Vögel mit Gesangsfrequenzen, die weit über den Frequenzen von Verkehrsgeräuschen liegen, weniger lärmempfindlich sind. Diesen Ergebnissen zufolge ist die akustische Überdeckung von Vogelgesang in den Frequenzbereichen von Straßenlärm einer der Mechanismen, durch welche Singvogeldichten entlang von Straßen negativ beeinträchtigt werden.

Conflict between genetic and phenotypic differentiation: the evolutionary history of a 'lost and rediscovered' shorebird.

Understanding and resolving conflicts between phenotypic and genetic differentiation is central to evolutionary research. While phenotypically monomorphic species may exhibit deep genetic divergences, some morphologically distinct taxa lack notable genetic differentiation. Here we conduct a molecular investigation of an enigmatic shorebird with a convoluted taxonomic history, the White-faced Plover (Charadrius alexandrinus dealbatus), widely regarded as a subspecies of the Kentish Plover (C. alexandrinus). Described as distinct in 1863, its name was consistently misapplied in subsequent decades until taxonomic clarification ensued in 2008. Using a recently proposed test of species delimitation, we reconfirm the phenotypic distinctness of dealbatus. We then compare three mitochondrial and seven nuclear DNA markers among 278 samples of dealbatus and alexandrinus from across their breeding range and four other closely related plovers. We fail to find any population genetic differentiation between dealbatus and alexandrinus, whereas the other species are deeply diverged at the study loci. Kentish Plovers join a small but growing list of species for which low levels of genetic differentiation are accompanied by the presence of strong phenotypic divergence, suggesting that diagnostic phenotypic characters may be encoded by few genes that are difficult to detect. Alternatively, gene expression differences may be crucial in producing different phenotypes whereas neutral differentiation may be lagging behind.

Habitat shifts in the evolutionary history of a Neotropical flycatcher lineage from forest and open landscapes.

BackgroundLittle is known about the role ecological shifts play in the evolution of Neotropical radiations that have colonized a variety of environments. We here examine habitat shifts in the evolutionary history of Elaenia flycatchers, a Neotropical bird lineage that lives in a range of forest and open habitats. We evaluate phylogenetic relationships within the genus based on mitochondrial and nuclear DNA sequence data, and then employ parsimony-based and Bayesian methods to reconstruct preferences for a number of habitat types and migratory behaviour throughout the evolutionary history of the genus. Using a molecular clock approach, we date the most important habitat shifts.ResultsOur analyses resolve phylogenetic relationships among Elaenia species and confirm several species associations predicted by morphology while furnishing support for other taxon placements that are in conflict with traditional classification, such as the elevation of various Elaenia taxa to species level. While savannah specialism is restricted to one basal clade within the genus, montane forest was invaded from open habitat only on a limited number of occasions. Riparian growth may have been favoured early on in the evolution of the main Elaenia clade and subsequently been deserted on several occasions. Austral long-distance migratory behaviour evolved on several occasions.ConclusionAncestral reconstructions of habitat preferences reveal pronounced differences not only in the timing of the emergence of certain habitat preferences, but also in the frequency of habitat shifts. The early origin of savannah specialism in Elaenia highlights the importance of this habitat in Neotropical Pliocene and late Miocene biogeography. While forest in old mountain ranges such as the Tepuis and the Brazilian Shield was colonized early on, the most important colonization event of montane forest was in conjunction with Pliocene Andean uplift. Riparian habitats may have played an important role in facilitating habitat shifts by birds expanding up the mountains along streams and adapting to newly emerging montane forest habitat.

Plumage patterns are good indicators of taxonomic diversity, but not of phylogenetic affinities, in Australian grasswrens Amytornis (Aves: Maluridae)

The grasswrens (Maluridae: Amytornis) are elusive songbirds from the arid zones of Australia. Although some other Australian bird genera are also largely restricted to arid regions, none show the level of localized taxonomic diversity seen in Amytornis. Furthermore, their cryptic plumage patterns provide excellent camouflage but make it difficult to determine whether shared patterns reflect phylogenetic relationships or adaptations to similar terrain. To resolve the systematics and patterns of ecological diversification within Amytornis, we here present the results of a phylogenetic analysis of mitochondrial and nuclear multi-locus data for all recognized species and most subspecies, using traditional concatenation-based methods as well as a coalescent-based species-tree approach. Phylogenetic patterns retrieved by the species-tree approach were highly congruent with traditional methods, although branch support was generally higher in concatenation-based analysis, suggesting that species-tree methods may furnish more conservative results. In terms of identifying taxonomic diversity there was good concordance between plumage-based assessments and DNA distances. The same concordance was not found when comparing plumage-based and DNA-based predictions of phylogenetic relationships. Four primary lineages were identified: (a) barbatus; (b) merrotsyi; (c) the textilis complex, purnelli, ballarae, goyderi and housei; and (d) woodwardi, dorotheae, and the striatus complex. There was no robust resolution of relationships between lineages. It appears that in Amytornis, plumage differentiation between discrete populations is taxonomically significant, and not greatly influenced by ecophenotypic variation. However, at the deeper phylogenetic level, similar suites of plumage characters may be phylogenetically uninformative because of homoplasy. The study reveals higher levels of taxonomic diversity in Amytornis than previously recognized, with many taxa being highly localized. Such extensive short range endemism is mainly encountered in poorly-dispersing invertebrates and is unique in Australian birds. The identification here of the additional restricted range taxa has important conservation implications.

Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes

Parasite host switches may trigger disease emergence, but prehistoric host ranges are often unknowable. Lymphatic filariasis and loiasis are major human diseases caused by the insect-borne filarial nematodes Brugia, Wuchereria and Loa. Here we show that the genomes of these nematodes and seven tropical bird lineages exclusively share a novel retrotransposon, AviRTE, resulting from horizontal transfer (HT). AviRTE subfamilies exhibit 83–99% nucleotide identity between genomes, and their phylogenetic distribution, paleobiogeography and invasion times suggest that HTs involved filarial nematodes. The HTs between bird and nematode genomes took place in two pantropical waves, >25–22 million years ago (Myr ago) involving the Brugia/Wuchereria lineage and >20–17 Myr ago involving the Loa lineage. Contrary to the expectation from the mammal-dominated host range of filarial nematodes, we hypothesize that these major human pathogens may have independently evolved from bird endoparasites that formerly infected the global breadth of avian biodiversity.

Major analytical and conceptual shortcomings in a recent taxonomic revision of the Procellariiformes – a reply to Penhallurick and Wink (2004)

Abstract A recent taxonomic revision of Procellariiformes by Penhallurick and Wink (2004) based on cytochrome b sequence data contains analytical and conceptual flaws that compromise the validity of the taxonomic recommendations. We identify two major shortcomings in the work. First, we question the practice of basing taxonomic recommendations on tree clades that receive no statistical support, and also highlight inconsistences n the tree-searching methods used. Second, we question Penhallurick and Winks claim to be following the multidimensional biological species concept, because they have put forward taxonomic proposals that violate this species concept (as well as the phylogenetic species concept). We discuss these analytical and conceptual shortcomings and make recommendations against the taxonomic rearrangements proposed by Penhallurick and Wink.

DNA evidence shows vocalizations to be a better indicator of taxonomic limits than plumage patterns in Zimmerius tyrant-flycatchers

We investigated mitochondrial and nuclear DNA in the small tyrant-flycatcher genus Zimmerius (Tyrannidae) and show that molecular data are in strong disagreement with morphology-based taxonomy, but in good concordance with vocal characters. Our molecular data identified two independent cases of well-supported polyphyletic species arrangements within this genus that indicate the following taxonomic changes: elevation of Z. acer and Z. albigularis to species level, separation of northern populations of Z. chrysops as a species and inclusion of southern populations of Z. chrysops into Z. viridiflavus. Although polyphyly has rarely been encountered in bird systematics it has previously been shown for two other tyrannid genera and suggests that tyrannid taxonomy may be poorly resolved, presumably as a consequence of the conserved plumage patterns observed in many tyrannid genera. Our study suggests that vocalizations can be a better indicator of taxonomic limits than plumage pattern in tyrannids.

Genetic introgression, incomplete lineage sorting and faulty taxonomy create multiple cases of polyphyly in a montane clade of tyrant-flycatchers (Elaenia, Tyrannidae)

Species‐level paraphyly and polyphyly are pervasive phenomena in modern phylogenetic research and can be due to a number of factors. We explore a complicated pattern of nuclear and mitochondrial polyphyly in montane Neotropical Elaenia flycatchers. Using a combination of phylogenetic and population genetic methods, we demonstrate that no single factor is sufficient to account for this pattern of polyphyly, and that it is likely based on an interplay of three different factors: (i) faulty taxonomy which has led to the recognition of two polyphyletic species that are better classified as four biological species; (ii) a late Pleistocene hybridization event that resulted in two morphologically and ecologically distinct species sharing extremely similar mitochondrial DNA but distinct nuclear DNA profiles; and (iii) incomplete lineage sorting in a nuclear marker that results in a polyphyletic placement of species that are otherwise well‐differentiated in mitochondrial DNA, morphology and ecology. Additionally, we demonstrate that the two clades of montane Elaenia exhibit a reverse pattern of mitochondrial and nuclear diversity, with high mitochondrial and low nuclear genetic diversity in one clade and vice versa in the other clade. A possible cause for this pattern is differences in population histories, with large panmictic population structures being conducive to the retention of ancient nuclear polymorphisms in Elaenia albiceps chilensis.

A re-appraisal of species diversity within the Australian grasswrens Amytornis (Aves: Maluridae)

The Australian grasswrens (Amytornis) comprise a genus of cryptically plumaged species inhabiting the arid regions of southern, western, central, and northern Australia. Isolated, fragmented populations characterise the distributional pattern of several species, whereas others appear to show ecophenotypic clinal variation in plumage patterns. These features have made the species-level taxonomy of the genus a matter of ongoing debate. We undertook qualitative considerations of morphological, biogeographical and ecological features in combination with quantitative DNA distance measures from published studies, to provide a comprehensive species level revision of Amytornis. In addition to the ten species recognised by Schodde and Mason (1999) (housei, textilis, goyderi, purnelli, ballarae, merrotsyi, woodwardi, dorotheae, striatus, barbatus), we also recognise as species the following: modestus, rowleyi, oweni and whitei. These fourteen species are placed into four subgenera: Amytornis, Magnamytis, Maluropsis...