Early birds are sexy: male age, dawn song and extrapair paternity in blue tits, Cyanistes (formerly Parus) caeruleus

Sexual selection theory predicts that signals reflecting the relative quality of individuals should be used in mate choice. Females could base their choice of copulation partners on male secondary sexual traits that honestly signal male age, as predicted by the age-based indicator mechanism. Studies have shown that female blue tits prefer older males and that aspects of dawn song reflect male quality, but it remains unknown whether dawn song characteristics correlate with male age. We compared dawn song characteristics of second-year (SY) and older (ASY) male blue tits (cross-sectional analysis), and tested for age-related changes within individuals (longitudinal analysis) and differential overwinter survival of SY males. We further investigated the relation between dawn song and paternity gain and loss. We found that ASY male blue tits began to sing earlier relative to sunrise than did SY males. This difference in the onset of dawn singing was due to age-related changes in individual performance rather than differential survival of individuals with varying expression of the trait. Males that began to sing earlier at dawn had more mating partners, and were more likely to gain extrapair paternity. Our findings suggest that the onset of dawn song can provide a simple mechanism for females to assess the relative quality of their mate and of neighbouring males. We propose that females use the onset of singing as a cue for their choice of extrapair partners. (c) 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Evidence for repeated independent evolution of migration in the largest family of bats

Background: How migration evolved represents one of the most poignant questions in evolutionary biology. While studies on the evolution of migration in birds are well represented in the literature, migration in bats has received relatively little attention. Yet, more than 30 species of bats are known to migrate annually from breeding to non-breeding locations. Our study is the first to test hypotheses on the evolutionary history of migration in bats using a phylogenetic framework. Methods and Principal Findings: In addition to providing a review of bat migration in relation to existing hypotheses on the evolution of migration in birds, we use a previously published supertree to formulate and test hypotheses on the evolutionary history of migration in bats. Our results suggest that migration in bats has evolved independently in several lineages potentially as the need arises to track resources (food, roosting site) but not through a series of steps from short- to long-distance migrants, as has been suggested for birds. Moreover, our analyses do not indicate that migration is an ancestral state but has relatively recently evolved in bats. Our results also show that migration is significantly less likely to evolve in cave roosting bats than in tree roosting species. Conclusions and Significance: This is the first study to provide evidence that migration has evolved independently in bat lineages that are not closely related. If migration evolved as a need to track seasonal resources or seek adequate roosting sites, climate change may have a pivotal impact on bat migratory habits. Our study provides a strong framework for future research on the evolution of migration in chiropterans. © 2009 Bisson et al.

Migratory navigation in birds: new opportunities in an era of fast-developing tracking technology

Birds have remained the dominant model for studying the mechanisms of animal navigation for decades, with much of what has been discovered coming from laboratory studies or model systems. The miniaturisation of tracking technology in recent years now promises opportunities for studying navigation during migration itself (migratory navigation) on an unprecedented scale. Even if migration tracking studies are principally being designed for other purposes, we argue that attention to salient environmental variables during the design or analysis of a study may enable a host of navigational questions to be addressed, greatly enriching the field. We explore candidate variables in the form of a series of contrasts (e. g. land vs ocean or night vs day migration), which may vary naturally between migratory species, populations or even within the life span of a migrating individual. We discuss how these contrasts might help address questions of sensory mechanisms, spatiotemporal representational strategies and adaptive variation in navigational ability. We suggest that this comparative approach may help enrich our knowledge about the natural history of migratory navigation in birds.

Predicting the impacts of climate change on the distribution of threatened forest-restricted birds in Madagascar

The greatest common threat to birds in Madagascar has historically been from anthropogenic deforestation. During recent decades, global climate change is now also regarded as a significant threat to biodiversity. This study uses Maximum Entropy species distribution modeling to explore how potential climate change could affect the distribution of 17 threatened forest endemic bird species, using a range of climate variables from the Hadley Center's HadCM3 climate change model, for IPCC scenario B2a, for 2050. We explore the importance of forest cover as a modeling variable and we test the use of pseudo-presences drawn from extent of occurrence distributions. Inclusion of the forest cover variable improves the models and models derived from real-presence data with forest layer are better predictors than those from pseudo-presence data. Using real-presence data, we analyzed the impacts of climate change on the distribution of nine species. We could not predict the impact of climate change on eight species because of low numbers of occurrences. All nine species were predicted to experience reductions in their total range areas, and their maximum modeled probabilities of occurrence. In general, species range and altitudinal contractions follow the reductive trend of the Maximum presence probability. Only two species (Tyto soumagnei and Newtonia fanovanae) are expected to expand their altitude range. These results indicate that future availability of suitable habitat at different elevations is likely to be critical for species persistence through climate change. Five species (Eutriorchis astur, Neodrepanis hypoxantha, Mesitornis unicolor, Euryceros prevostii, and Oriola bernieri) are probably the most vulnerable to climate change. Four of them (E. astur, M. unicolor, E. prevostii, and O. bernieri) were found vulnerable to the forest fragmentation during previous research. Combination of these two threats in the future could negatively affect these species in a drastic way. Climate change is expected to act differently on each species and it is important to incorporate complex ecological variables into species distribution models.

True navigation in birds: from quantum physics to global migration

Birds are capable of true navigation, the ability to return to a known goal from a place they have never visited before. This is demonstrated most spectacularly during the vast migratory journeys made by these animals year after year, often between continents and occasionally global in nature. However, it remains one of the great unanswered questions in science, despite more than 50 years of research in this field. Nevertheless, the study of true navigation in birds has made significant advances in the previous 20 years, in part thanks to the integration of many disciplines outside its root in behavioural biology, to address questions of neurobiology, molecular aspects, and the physics of sensory systems and environmental cues involved in bird navigation, often involving quantum physics. However, true navigation remains a controversial field, with many conflicting and confusing results making interpretation difficult, particularly for those outside or new to the field. Unlike many general texts on migration, which avoid discussion of these issues, this review will present these conflicting findings and assess the state of the field of true navigation during bird migration.

Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy

Here, we analyze the complete coding sequences of all recognized tick-borne flavivirus species, including Gadgets Gully, Royal Farm and Karshi virus, seabird-associated flaviviruses, Kadam virus and previously uncharacterized isolates of Kyasanur Forest disease virus and Omsk hemorrhagic fever virus. Significant taxonomic improvements are proposed, e.g. the identification of three major groups (mammalian, seabird and Kadam tick-borne flavivirus groups), the creation of a new species (Karshi virus) and the assignment of Tick-borne encephalitis and Louping ill viruses to a unique species (Tick-borne encephalitis virus) including four viral types (i.e. Western Tick-borne encephalitis virus, Eastern Tick-borne encephalitis virus, Turkish sheep Tick-borne encephalitis virus and Louping ill Tick-borne encephalitis virus). The analyses also suggest a complex relationship between viruses infecting birds and those infecting mammals. Ticks that feed on both categories of vertebrates may constitute the evolutionary bridge between the three distinct identified lineages.

Evolution of Dendrocolaptes platyrostris (Aves: Furnariidae) between the South American open vegetation corridor and the Atlantic forest

The open vegetation corridor of South America is a region dominated by savanna biomes. It contains forests (i.e. riverine forests) that may act as corridors for rainforest specialists between the open vegetation corridor and its neighbouring biomes (i.e. the Amazonian and Atlantic forests). A prediction for this scenario is that populations of rainforest specialists in the open vegetation corridor and in the forested biomes show no significant genetic divergence. We addressed this hypothesis by studying plumage and genetic variation of the Planalto woodcreeper Dendrocolaptes platyrostris Spix (1824) (Aves: Furnariidae), a forest specialist that occurs in both open habitat and in the Atlantic forest. The study questions were: (1) is there any evidence of genetic continuity between populations of the open habitat and the Atlantic forest and (2) is plumage variation congruent with patterns of neutral genetic structure or with ecological factors related to habitat type? We used cytochrome b and mitochondrial DNA control region sequences to show that D. platyrostris is monophyletic and presents substantial intraspecific differentiation. We found two areas of plumage stability: one associated with Cerrado and the other associated with southern Atlantic Forest. Multiple Mantel tests showed that most of the plumage variation followed the transition of habitats but not phylogeographical gaps, suggesting that selection may be related to the evolution of the plumage of the species. The results were not compatible with the idea that forest specialists in the open vegetation corridor and in the Atlantic forest are linked at the population level because birds from each region were not part of the same genetic unit. Divergence in the presence of gene flow across the ecotone between both regions might explain our results. Also, our findings indicate that the southern Atlantic forest may have been significantly affected by Pleistocene climatic alteration, although such events did not cause local extinction of most taxa, as occurred in other regions of the globe where forests were significantly affected by global glaciations. Finally, our results neither support plumage stability areas, nor subspecies as full species. (C) 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 801-820.

Genomic analyses and cloning of novel chicken natriuretic peptide genes reveal new insights into natriuretic peptide evolution

The natriuretic peptide (NP) family consists of multiple subtypes in teleosts, including atrial, B-type, ventricular, and C-type NPs (ANP, BNP, VNP, CNP-1–4, respectively), but only ANP, BNP, CNP-3, and CNP-4 have been identified in tetrapods. As part of understanding the molecular evolution of NPs in the tetrapod lineage, we identified NP genes in the chicken genome. Previously, only BNP and CNP-3 have been identified in birds, but we characterized two new chicken NP genes by cDNA cloning, synteny and phylogenetic analyses. One gene is an orthologue of CNP-1, which has only ever been reported in teleostei and bichir. The second gene could not be assigned to a particular NP subtype because of high sequence divergence and was named renal NP (RNP) due to its predominant expression in the kidney. CNP-1 mRNA was only detected in brain, while CNP-3 mRNA was expressed in kidney, heart, and brain. In the developing embryo, BNP and RNP transcripts were most abundant 24 h post-fertilization, while CNP mRNA increased in a stage-dependant manner. Synthetic chicken RNP stimulated an increase in cGMP production above basal level in chicken kidney membrane preparations and caused a potent dose-dependant vasodilation of pre-constricted dorsal aortic rings. From conserved chromosomal synteny, we propose that the CNP-4 and ANP genes have been lost in chicken, and that RNP may have evolved from a VNP-like gene. Furthermore, we have demonstrated for the first time that CNP-1 is retained in the tetrapod lineage.

Molecular cloning of natriuretic peptides from the heart of reptiles : loss of ANP in diapsid reptiles and birds

Atrial natriuretic peptide (ANP) and B-type NP (BNP) are hormones involved in homeostatic control of body fluid and cardiovascular regulation. Both ANP and BNP have been cloned from the heart of mammals, amphibians, and teleost fishes, while an additional cardiac peptide, ventricular NP, has been found in selected species of teleost fish. However, in chicken, BNP is the primary cardiac peptide identified thus far. In contrast, the types of NP/s present in the reptilian heart are unknown, representing a considerable gap in our understanding of NP evolution. In the present study, we cloned and sequenced a BNP cDNA from the atria of representative species of reptile, including crocodile, lizard, snake, and tortoise. In addition, we cloned BNP from the pigeon atria. The reptilian and pigeon BNP cDNAs had ATTTA repeats in the 3′ untranslated region, as observed in all vertebrate BNP mRNAs. A high sequence homology was evident when comparing reptile and pigeon preproBNP with the previously identified chicken preproBNP. In particular, the predicted mature BNP-29 was identical between crocodile, tortoise, and chicken, with pigeon having a single amino acid substitution; lizard and snake BNP had seven and nine substitutions, respectively. Furthermore, an ANP cDNA could only be cloned from the tortoise atria. Since ANP was not isolated from the heart of any non-chelonian reptile and appears to be absent in birds, we propose that the ANP gene has been lost after branching of the turtles in the amniote line. This data provides new avenues for research on NP function in reptiles.

Ecological and life-history factors influencing the evolution of maternal antibody allocation : a phylogenetic comparison

Maternally derived yolk antibodies provide neonates with immune protection in early life at negligible cost to mothers. However, developmental effects on the neonate's future immunity are potentially costly and thus could limit yolk antibody deposition. The benefits to neonatal immunity must be balanced against costs, which may depend on neonate vulnerability to pathogens, developmental trajectories and the immunological strategies best suited to a species' pace of life. We measured yolk antibodies and life-history features of 23 species of small Neotropical birds and assessed the evidence for each of several hypotheses for life history and ecological effects on the evolution of yolk antibody levels. Developmental period and yolk antibodies are negatively related, which possibly reflect the importance of humoral immune priming through antigen exposure, and selection to avoid autoimmunity, in species with a slower pace of life. There is also a strong relationship between body size and yolk antibody concentration, suggesting that larger species are architecturally equipped to produce and transfer higher concentrations of antibodies. These results suggest that developmental effects of maternally derived antibodies, such as imprinting effects on B-cell diversity or autoimmune effects, are important and deserve more consideration in future research.

Molecular biology of natriuretic peptides in reptiles and birds

The heart produces natriuretic peptides that are critical regulators of blood pressure and renal function. This study examined the molecular evolution of natriuretic peptides in vertebrates and discovered novel forms of the peptides in birds. The research outcomes advanced our knowledge of the importance of these peptides in animal physiology.

The developmental stress hypothesis: A special case of the evolution of condition-dependent sexual traits

The idea that sexually selected traits might be condition dependent is far from novel (Zahavi 1975); however, the developmental stress hypothesis was proposed as a special case because of a highly plausible mechanism: the development of the neural circuits controlling song output coincides with a period of time during which developing birds are likely to be susceptible to stress. The elegant aspect of the hypothesis is that the mechanism is defined and effects can be readily tested (Nowicki et al. 1998; Buchanan et al. 2003). Compared with more general hypotheses about the evolution of condition-dependent sexual traits (Buchanan 2000), the second particularly interesting aspect of the developmental stress hypothesis is that, in some species, individuals may suffer historical markers of stress. This is because in species with a fixed period for neural growth and song learning, there is no possibility for compensation in later life for stress experienced during early development. Females using such a marker of stress may benefit by obtaining a partner whose other cognitive functions have not been impaired by stress.

Molecular sex-typing in shorebirds: a review of an essential method for research in evolution, ecology and conservation

Knowing the correct sex of individuals is essential both for research in evolutionary ecology and for practical conservation. Recent molecular advances have produced cheap, quick and reliable methods for sexing birds including chicks, juveniles, immatures and adults. Shorebird researchers have not yet fully utilised these advances. Here we provide an overview of work in this area to date with two objectives: (i) to review the major applications of molecular sexing and findings of shorebird research so far, and (ii) to provide an essential guide on how to carry out molecular sexing using current methods whilst avoiding methodological pitfalls. We encourage shorebird researchers to make better use of molecular sex-typing techniques in studies of conservation, migration, foraging ecology and breeding behaviour.

Convergent evolution in locomotory patterns of flying and swimming animals

Locomotion is one of the major energetic costs faced by animals and various strategies have evolved to reduce its cost. Birds use interspersed periods of flapping and gliding to reduce the mechanical requirements of level flight while undergoing cyclical changes in flight altitude, known as undulating flight. Here we equipped free-ranging marine vertebrates with accelerometers and demonstrate that gait patterns resembling undulating flight occur in four marine vertebrate species comprising sharks and pinnipeds. Both sharks and pinnipeds display intermittent gliding interspersed with powered locomotion. We suggest, that the convergent use of similar gait patterns by distinct groups of animals points to universal physical and physiological principles that operate beyond taxonomic limits and shape common solutions to increase energetic efficiency. Energetically expensive large-scale migrations performed by many vertebrates provide common selection pressure for efficient locomotion, with potential for the convergence of locomotory strategies by a wide variety of species.

The evolution of nitric oxide signalling in vertebrate blood vessels

Nitric oxide is one of the most important signalling molecules involved in the regulation of physiological function. It first came to prominence when it was discovered that the vascular endothelium of mammals synthesises and releases nitric oxide (NO) to mediate a potent vasodilation. Subsequently, it was shown that NO is synthesised in the endothelium by a specific isoform of nitric oxide synthase (NOS) called NOS3. Following this discovery, it was assumed that an endothelial NO/NOS3 system would be present in all vertebrate blood vessels. This review will discuss the latest genomic, anatomical and physiological evidence which demonstrates that an endothelial NO/NOS3 signalling is not ubiquitous in non-mammalian vertebrates, and that there have been key evolutionary steps that have led to the endothelial NO signalling system being a regulatory system found only in reptiles, birds and mammals. Furthermore, the emerging role of nitrite as an endocrine source of NO for vascular regulation is discussed.