The effect of climate change on avian offspring production: A global meta-analysis.

Climate change affects timing of reproduction in many bird species, but few studies have investigated its influence on annual reproductive output. Here, we assess changes in the annual production of young by female breeders in 201 populations of 104 bird species (N = 745,962 clutches) covering all continents between 1970 and 2019. Overall, average offspring production has declined in recent decades, but considerable differences were found among species and populations. A total of 56.7% of populations showed a declining trend in offspring production (significant in 17.4%), whereas 43.3% exhibited an increase (significant in 10.4%). The results show that climatic changes affect offspring production through compounded effects on ecological and life history traits of species. Migratory and larger-bodied species experienced reduced offspring production with increasing temperatures during the chick-rearing period, whereas smaller-bodied, sedentary species tended to produce more offspring. Likewise, multi-brooded species showed increased breeding success with increasing temperatures, whereas rising temperatures were unrelated to reproductive success in single-brooded species. Our study suggests that rapid declines in size of bird populations reported by many studies from different parts of the world are driven only to a small degree by changes in the production of young.

Female and male Leach's Storm Petrels (Hydrobates leucorhous) pursue different foraging strategies during the incubation period.

Reproduction in procellariiform birds is characterized by a single egg clutch, slow development, a long breeding season and obligate biparental care. Female Leach's Storm Petrels Hydrobates leucorhous, nearly monomorphic members of this order, produce eggs that are between 20 and 25% of adult body weight. We tested whether female foraging behaviour differs from male foraging behaviour during the ~ 44-day incubation period across seven breeding colonies in the Northwest Atlantic. Over six breeding seasons, we used a combination of Global Positioning System and Global Location Sensor devices to measure characteristics of individual foraging trips during the incubation period. Females travelled significantly greater distances and went farther from the breeding colony than did males on individual foraging trips. For both sexes, the longer the foraging trip, the greater the distance. Independent of trip duration, females travelled farther, and spent a greater proportion of their foraging trips prospecting widely as defined by behavioural categories derived from a Hidden Markov Model. For both sexes, trip duration decreased with date. Sex differences in these foraging metrics were apparently not a consequence of morphological differences or spatial segregation. Our data are consistent with the idea that female foraging strategies differed from male foraging strategies during incubation in ways that would be expected if females were still compensating for egg formation.

Meta-analysis of major histocompatibility complex (MHC) class IIA reveals polymorphism and positive selection in many vertebrate species.

Pathogen-mediated selection and sexual selection are important drivers of evolution. Both processes are known to target genes of the major histocompatibility complex (MHC), a gene family encoding cell-surface proteins that display pathogen peptides to the immune system. The MHC is also a model for understanding processes such as gene duplication and trans-species allele sharing. The class II MHC protein is a heterodimer whose peptide-binding groove is encoded by an MHC-IIA gene and an MHC-IIB gene. However, our literature review found that class II MHC papers on infectious disease or sexual selection included IIA data only 18% and 9% of the time, respectively. To assess whether greater emphasis on MHC-IIA is warranted, we analysed MHC-IIA sequence data from 50 species of vertebrates (fish, amphibians, birds, mammals) to test for polymorphism and positive selection. We found that the number of MHC-IIA alleles within a species was often high, and covaried with sample size and number of MHC-IIA genes assayed. While MHC-IIA variability tended to be lower than that of MHC-IIB, the difference was only ~25%, with ~3 fewer IIA alleles than IIB. Furthermore, the unexpectedly high MHC-IIA variability showed clear signatures of positive selection in most species, and positive selection on MHC-IIA was stronger in fish than in other surveyed vertebrate groups. Our findings underscore that MHC-IIA can be an important target of selection. Future studies should therefore expand the characterization of MHC-IIA at both allelic and genomic scales, and incorporate MHC-IIA into models of fitness consequences of MHC variation.

Divergence between genes but limited allelic polymorphism in two MHC class II A genes in Leach's storm-petrels Oceanodroma leucorhoa.

The major histocompatibility complex (MHC) is critical to host-pathogen interactions. Class II MHC is a heterodimer, with α and ß subunits encoded by different genes. The peptide-binding groove is formed by the first domain of both subunits (α1 and ß1), but studies of class II variation or natural selection focus primarily on the ß subunit and II B genes. We explored MHC II A in Leach's storm-petrel, a seabird with two expressed, polymorphic II B genes. We found two II A genes, Ocle-DAA and Ocle-DBA, in contrast to the single II A gene in chicken and duck. In exon 2 which encodes the α1 domain, the storm-petrel II A genes differed strongly from each other but showed little within-gene polymorphism in 30 individuals: just one Ocle-DAA allele, and three Ocle-DBA alleles differing from each other by single non-synonymous substitutions. In a comparable sample, the two II B genes had nine markedly diverged alleles each. Differences between the α1 domains of Ocle-DAA and Ocle-DBA showed signatures of positive selection, but mainly at non-peptide-binding site (PBS) positions. In contrast, positive selection within and between the II B genes corresponded to putative PBS codons. Phylogenetic analysis of the conserved α2 domain did not reveal deep or well-supported lineages of II A genes in birds, in contrast to the pronounced differentiation of DQA, DPA, and DRA isotypes in mammals. This uncertain homology complicates efforts to compare levels of functional variation and modes of evolution of II A genes across taxa.

Annual global mean temperature explains reproductive success in a marine vertebrate from 1955 to 2010.

The salient feature of anthropogenic climate change over the last century has been the rise in global mean temperature. However, global mean temperature is not used as an explanatory variable in studies of population-level response to climate change, perhaps because the signal-to-noise ratio of this gross measure makes its effect difficult to detect in any but the longest of datasets. Using a population of Leach's storm-petrels breeding in the Bay of Fundy, we tested whether local, regional, or global temperature measures are the best index of reproductive success in the face of climate change in species that travel widely between and within seasons. With a 56-year dataset, we found that annual global mean temperature (AGMT) was the single most important predictor of hatching success, more so than regional sea surface temperatures (breeding season or winter) and local air temperatures at the nesting colony. Storm-petrel reproductive success showed a quadratic response to rising temperatures, in that hatching success increased up to some critical temperature, and then declined when AGMT exceeded that temperature. The year at which AGMT began to consistently exceed that critical temperature was 1988. Importantly, in this population of known-age individuals, the impact of changing climate was greatest on inexperienced breeders: reproductive success of inexperienced birds increased more rapidly as temperatures rose and declined more rapidly after the tipping point than did reproductive success of experienced individuals. The generality of our finding that AGMT is the best predictor of reproductive success in this system may hinge on two things. First, an integrative global measure may be best for species in which individuals move across an enormous spatial range, especially within seasons. Second, the length of our dataset and our capacity to account for individual- and age-based variation in reproductive success increase our ability to detect a noisy signal.

Gene duplication and divergence produce divergent MHC genotypes without disassortative mating.

Genes of the major histocompatibility complex (MHC) exhibit heterozygote advantage in immune defence, which in turn can select for MHC-disassortative mate choice. However, many species lack this expected pattern of MHC-disassortative mating. A possible explanation lies in evolutionary processes following gene duplication: if two duplicated MHC genes become functionally diverged from each other, offspring will inherit diverse multilocus genotypes even under random mating. We used locus-specific primers for high-throughput sequencing of two expressed MHC Class II B genes in Leach's storm-petrels, Oceanodroma leucorhoa, and found that exon 2 alleles fall into two gene-specific monophyletic clades. We tested for disassortative vs. random mating at these two functionally diverged Class II B genes, using multiple metrics and different subsets of exon 2 sequence data. With good statistical power, we consistently found random assortment of mates at MHC. Despite random mating, birds had MHC genotypes with functionally diverged alleles, averaging 13 amino acid differences in pairwise comparisons of exon 2 alleles within individuals. To test whether this high MHC diversity in individuals is driven by evolutionary divergence of the two duplicated genes, we built a phylogenetic permutation model. The model showed that genotypic diversity was strongly impacted by sequence divergence between the most common allele of each gene, with a smaller additional impact of monophyly of the two genes. Divergence of allele sequences between genes may have reduced the benefits of actively seeking MHC-dissimilar mates, in which case the evolutionary history of duplicated genes is shaping the adaptive landscape of sexual selection.

Non-neutral evolution and reciprocal monophyly of two expressed Mhc class II B genes in Leach's storm-petrel.

The major histocompatibility complex (Mhc) is subject to pathogen-mediated balancing selection and can link natural selection with mate choice. We characterized two Mhc class II B loci in Leach's storm-petrel, Oceanodroma leucorhoa, focusing on exon 2 which encodes the portion of the protein that binds pathogen peptides. We amplified and sequenced exon 2 with locus-specific nested PCR and Illumina MiSeq using individually barcoded primers. Repeat genotyping of 78 single-locus genotypes produced identical results in 77 cases (98.7%). Sequencing of messenger RNA (mRNA) from three birds confirmed expression of both loci, consistent with the observed absence of stop codons or frameshifts in all alleles. In 48 birds, we found 9 and 12 alleles at the two loci, respectively, and all 21 alleles translated to unique amino acid sequences. Unlike many studies of duplicated Mhc genes, alleles of the two loci clustered into monophyletic groups. Consistent with this phylogenetic result, interlocus gene conversion appears to have affected only two short fragments of the exon. As predicted under a paradigm of pathogen-mediated selection, comparison of synonymous and non-synonymous substitution rates found evidence of a history of positive selection at putative peptide binding sites. Overall, the results suggest that the gene duplication event leading to these two loci is not recent and that point mutations and positive selection on the peptide binding sites may be the predominant forces acting on these genes. Characterization of these loci sets the stage for population-level work on the evolutionary ecology of Mhc in this species.

Sequence-based evidence for major histocompatibility complex-disassortative mating in a colonial seabird.

The major histocompatibility complex (MHC) is a polymorphic gene family associated with immune defence, and it can play a role in mate choice. Under the genetic compatibility hypothesis, females choose mates that differ genetically from their own MHC genotypes, avoiding inbreeding and/or enhancing the immunocompetence of their offspring. We tested this hypothesis of disassortative mating based on MHC genotypes in a population of great frigatebirds (Fregata minor) by sequencing the second exon of MHC class II B. Extensive haploid cloning yielded two to four alleles per individual, suggesting the amplification of two genes. MHC similarity between mates was not significantly different between pairs that did (n = 4) or did not (n = 42) exhibit extra-pair paternity. Comparing all 46 mated pairs to a distribution based on randomized re-pairings, we observed the following (i): no evidence for mate choice based on maximal or intermediate levels of MHC allele sharing (ii), significantly disassortative mating based on similarity of MHC amino acid sequences, and (iii) no evidence for mate choice based on microsatellite alleles, as measured by either allele sharing or similarity in allele size. This suggests that females choose mates that differ genetically from themselves at MHC loci, but not as an inbreeding-avoidance mechanism.

Nest sanitation behavior does not increase the likelihood of parasitic egg rejection in herring gulls.

Birds' behavioral response to brood parasitism can be influenced not only by evolution but also by context and individual experience. This could include nest sanitation, in which birds remove debris from their nests. Ultimately, nest sanitation behavior might be an evolutionary precursor to the rejection of parasitic eggs. Proximately, the context or experience of performing nest sanitation behavior might increase the detection or prime the removal of parasitic eggs, but evidence to date is limited. We tested incubation-stage nests of herring gulls Larus argentatus to ask whether nest sanitation increased parasitic egg rejection. In an initial set of 160 single-object experiments, small, red, blocky objects were usually rejected (18 of 20 nests), whereas life-sized, 3D-printed herring gull eggs were not rejected whether red (0 of 20) or the olive-tan base color of herring gull eggs (0 of 20). Next, we simultaneously presented a red, 3D-printed gull egg and a small, red block. These nests exhibited frequent nest sanitation (small, red block removed at 40 of 48 nests), but egg rejection remained uncommon (5 of those 40) and not significantly different from control nests (5 of 49) which received the parasitic egg but not the priming object. Thus, performance of nest sanitation did not shape individuals' responses to parasitism. Interestingly, parents were more likely to reject the parasitic egg when they were present as we approached the nest to add the experimental objects. Depending on the underlying mechanism, this could also be a case of experience creating variation in responses to parasitism.

Motivations for conserving urban biodiversity.

In a time of increasing urbanization, the fundamental value of conserving urban biodiversity remains controversial. How much of a fixed budget should be spent on conservation in urban versus nonurban landscapes? The answer should depend on the goals that drive our conservation actions, yet proponents of urban conservation often fail to specify the motivation for protecting urban biodiversity. This is an important shortcoming on several fronts, including a missed opportunity to make a stronger appeal to those who believe conservation biology should focus exclusively on more natural, wilder landscapes. We argue that urban areas do offer an important venue for conservation biology, but that we must become better at choosing and articulating our goals. We explored seven possible motivations for urban biodiversity conservation: preserving local biodiversity, creating stepping stones to nonurban habitat, understanding and facilitating responses to environmental change, conducting environmental education, providing ecosystem services, fulfilling ethical responsibilities, and improving human well-being. To attain all these goals, challenges must be faced that are common to the urban environment, such as localized pollution, disruption of ecosystem structure, and limited availability of land. There are, however, also challenges specific only to particular goals, meaning that different goals will require different approaches and actions. This highlights the importance of specifying the motivations behind urban biodiversity conservation. If the goals are unknown, progress cannot be assessed.

An individual-based model for the dispersal of Ixodes scapularis by ovenbirds and wood thrushes during fall migration.

Ixodes scapularis is responsible for the transmission of a variety of pathogens in North America, including Borrelia burgdorferi sensu stricto, Anaplasma phagocytophilum and Babesia microti. Songbirds have previously been described as agents of tick dispersal, and a combination of empirical data and modeling efforts have implicated songbirds in the range expansion of I. scapularis northward into Canada during spring bird migration. The role of fall bird migration has received comparatively less attention, particularly at a continental scale. The aim of the current research was to use a novel individual-based modeling approach (IBM) to investigate the role of southward migrating songbirds in the dispersal of I. scapularis within the continental United States. The IBM used in this research explicitly models dispersal by two extensively studied migrating songbird species, wood thrush Hylocichla mustelina and ovenbird Seiurus aurocapillus. Our IBM predicts the annual dispersal of more than four million ticks by H. mustelina and S. aurocapillus, notably into areas as far west as the Dakotas, and as far south as Central Alabama. Predicted dispersal locations include areas where the southern phenotype of I. scapularis dominates, suggestive of a possible mechanism for previously described unidirectional gene flow from north to south. In addition, the model demonstrates that three species-specific songbird traits - breeding range, migration timing, and propensity for tick attachment - each play a major role in the relative magnitude of tick dispersal by different songbird species. The pattern of I. scapularis dispersal predicted by this model suggests that migrating songbirds may have contributed to the range expansion of the tick historically, and may continue to do so presently and into the future, particularly as climate changes the geographic areas that are suitable for I. scapularis. Ultimately, widespread tick dispersal by migrating songbirds likely increases the human risk of Lyme disease and other tick-borne diseases in the United States.

Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host?

Many parasites show fidelity to a set of hosts in ecological time but not evolutionary time and the determinants of this pattern are poorly understood. Malarial parasites use vertebrate hosts for the asexual stage of their life cycle but use Dipteran hosts for the sexual stage. Despite the potential evolutionary importance of Dipteran hosts, little is known of their role in determining a parasite's access to vertebrate hosts. Here, we use an avian malarial system in Panama to explore whether mosquitoes act as an access filter that limits the range of vertebrate hosts used by particular parasite lineages. We amplified and sequenced Plasmodium mitochondrial DNA (mtDNA) from Turdus grayi (clay-coloured robin) and from mosquitoes at the same study site. We trapped and identified to species 123 141 female mosquitoes and completed polymerase chain reaction (PCR) screening for Plasmodium parasites in 435 pools of 20 mosquitoes per pool (8700 individuals total) spanning the 11 most common mosquito species. Our primers amplified nine Plasmodium lineages, whose sequences differed by 1.72%-10.0%. Phylogenetic analyses revealed partial clustering of lineages that co-occurred in mosquito hosts. However PAN3 and PAN6, the two primary parasite lineages of T. grayi, exhibited sequence divergence of 8.59% and did not cluster in the phylogeny. We detected these two lineages exclusively in mosquitoes from different genera - PAN3 was found only in Culex (Melanoconion) ocossa, and PAN6 was found only in Aedeomyia squamipennis. Furthermore, each of these two parasite lineages co-occurred in mosquitoes with other Plasmodium lineages that were not found in the vertebrate host T. grayi. Together, this evidence suggests that parasite-mosquito associations do not restrict the access of parasites to birds but instead may actually facilitate the switching of vertebrate hosts that occurs over evolutionary time.

Carotenoids and throat pouch coloration in the great frigatebird (Fregata minor).

Carotenoid pigments are a common source of red, orange, and yellow coloration in vertebrates. Animals cannot manufacture carotenoids and therefore must obtain them in their diet to produce carotenoid-based coloration. Male great frigatebirds (Fregata minor) display a bright red inflated gular pouch as part of their elaborate courtship display. The basis of this coloration until now has not been investigated. Using high-performance liquid chromatography (HPLC), we investigated the types and concentrations of carotenoids that great frigatebirds circulate in their plasma and whether male gular pouch coloration was carotenoid-based. Great frigatebird plasma collected during the breeding season contained three carotenoid pigments in dilute concentrations-tunaxanthin, zeaxanthin, and astaxanthin-with astaxanthin accounting for nearly 85% of the carotenoids present. Astaxanthin was the only carotenoid present in gular pouch tissue, but the concentration is the highest reported for any carotenoid-pigmented avian tissue. Throat pouch reflectance curves were measured with a UV-VIS spectrophotometer, revealing a complex pattern of one UV peak (approx. 360 nm), two absorption valleys (approx. 542 and 577 nm), followed by a plateau at approx 630 nm. The reflectance curve suggests a role for additional pigments, in particular hemoglobin, in the production of color in this ornament.

The rate of telomere loss is related to maximum lifespan in birds.

Telomeres are highly conserved regions of DNA that protect the ends of linear chromosomes. The loss of telomeres can signal an irreversible change to a cell's state, including cellular senescence. Senescent cells no longer divide and can damage nearby healthy cells, thus potentially placing them at the crossroads of cancer and ageing. While the epidemiology, cellular and molecular biology of telomeres are well studied, a newer field exploring telomere biology in the context of ecology and evolution is just emerging. With work to date focusing on how telomere shortening relates to individual mortality, less is known about how telomeres relate to ageing rates across species. Here, we investigated telomere length in cross-sectional samples from 19 bird species to determine how rates of telomere loss relate to interspecific variation in maximum lifespan. We found that bird species with longer lifespans lose fewer telomeric repeats each year compared with species with shorter lifespans. In addition, phylogenetic analysis revealed that the rate of telomere loss is evolutionarily conserved within bird families. This suggests that the physiological causes of telomere shortening, or the ability to maintain telomeres, are features that may be responsible for, or co-evolved with, different lifespans observed across species.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

Eggshells as hosts of bacterial communities: An experimental test of the antimicrobial egg coloration hypothesis.

Oviparous animals have evolved multiple defenses to prevent microbes from penetrating their eggs and causing embryo mortality. In birds, egg constituents such as lysozyme and antibodies defend against microbial infestation, but eggshell pigments might also impact survival of bacteria. If so, microbes could exert an important selective pressure on the evolution of eggshell coloration. In a previous lab experiment, eggshell protoporphyrin caused drastic mortality in cultures of Gram positive, but not Gram negative, bacteria when exposed to light. Here, we test this "photodynamic antimicrobial hypothesis" in a field experiment. In a paired experimental design, we placed sanitized brown, protoporphyrin-rich chicken eggs alongside white eggs that lack protoporphyrin. We deployed eggs for 48 hr without incubation, as can occur between laying and incubation, when microbial infection risk is highest. Eggs were placed on the open ground exposed to sunlight and in dark underground storm-petrel burrows. We predicted that the proportion of Gram-positive bacteria on brown eggs should be lower when exposed to sunlight than when kept in the dark, but we expected no such difference for white eggs. Although our data revealed variation in bacterial community composition, the proportion of Gram-positive bacteria on eggshells did not vary by egg color, and there was no interaction between egg color and location. Instead, Gram-positive bacteria were proportionally more common on eggs on the ground than eggs in burrows. Overall, our experiment did not support the photodynamic antimicrobial hypothesis. The diverse range of avian egg colors is generated by just two pigments, but over 10 hypotheses have been proposed for the evolution of eggshell color. If our results are generalizable, eggshell protoporphyrin might not play a substantial role in defending eggs against microbes, which narrows the field of candidate hypotheses for the evolution of avian eggshell coloration.

Microsatellite primers for relatedness and population structure in great frigatebirds (Pelecaniformes: Fregatidae).

Eighteen moderately polymorphic microsatellite loci were isolated and characterized for great frigatebirds Fregata minor. Polymorphism for the 12 dinucleotide and six tetranucleotide markers was assessed in 23 birds from a Hawaii population. Allelic diversity ranged from two to 12 (mean 5.9), with observed heterozygosity from 0.304 to 0.956 (mean 0.637). Three loci showed homozygote excess, possibly due to null alleles. One additional pair of loci exhibited strong gametic disequilibrium. Thus, at least 14 loci will be useful for studies of relatedness and population structure.

Inter-island movements and population differentiation in a pelagic seabird.

We used mark-resight data and amplified fragment length polymorphism (AFLP) markers to assess movements and gene flow between Central Pacific breeding colonies of the great frigatebird, Fregata minor. Of 715 adult frigatebirds marked on Tern Island and Johnston Atoll, 21.3% were resighted at other frigatebird colonies at least 582 km away. Mark-resight data indicated regular movement of males and females between Tern Island and Johnston Atoll (873 km apart), and less frequent movements to other islands; no birds marked on Tern or Johnston were seen on Christmas Island, but one was seen in the Philippines, 7627 km from where it was marked. Despite the regular occurrence of interisland movements, Bayesian analyses of AFLP data showed significant genetic differentiation between Tern Island and Johnston Atoll, and more pronounced differentiation between these two islands and the more distant Christmas Island. The AFLP profiles of three birds breeding on Tern Island fell within the profile-cluster typical for Christmas Island birds, both in a nonmetric multidimensional scaling analysis and in a population assignment test, suggesting dispersal events from Christmas Island to Tern Island. Several factors could explain the persistence of genetic structure despite frequent movements between colonies: many movements occurred during the nonbreeding season, many breeding-season movements did not involve mate-acquisition behaviours and individuals that do disperse may be selected against, as suggested by morphometric differences between colonies. The persistence of genetic structure among breeding colonies despite significant interisland movements suggests limits to the effectiveness of migration as a homogenizing force in this broadly distributed, extremely mobile species.