Independent evolution of intermediate bill widths in a seabird clade

16 pages, 5 figures, 5 tables, supplementary information https://doi.org/10.1007/s00438-021-01845-3.-- Availability of data and material: DNA sequences: GenBank accession numbers are provided in Table 1. All data are available in the manuscript or in the Supplementary information fileInterspecific introgression can occur between species that evolve rapidly within an adaptive radiation. Pachyptila petrels differ in bill size and are characterised by incomplete reproductive isolation, leading to interspecific gene flow. Salvin’s prion (Pachyptila salvini), whose bill width is intermediate between broad-billed (P. vittata) and Antarctic (P. desolata) prions, evolved through homoploid hybrid speciation. MacGillivray’s prion (P. macgillivrayi), known from a single population on St Paul (Indian Ocean), has a bill width intermediate between salvini and vittata and could also be the product of interspecies introgression or hybrid speciation. Recently, another prion population phenotypically similar to macgillivrayi was discovered on Gough (Atlantic Ocean), where it breeds 3 months later than vittata. The similarity in bill width between the medium-billed birds on Gough and macgillivrayi suggest that they could be closely related. In this study, we used genetic and morphological data to infer the phylogenetic position and evolutionary history of P. macgillivrayi and the Gough medium-billed prion relative other Pachyptila taxa, to determine whether species with medium bill widths evolved through common ancestry or convergence. We found that Gough medium-billed prions belong to the same evolutionary lineage as macgillivrayi, representing a new population of MacGillivray’s prion that originated through a colonisation event from St Paul. We show that macgillivrayi’s medium bill width evolved through divergence (genetic drift) and independently from that of salvini, which evolved through hybridisation (gene flow). This represents the independent convergence towards a similarly medium-billed phenotype. The newly discovered MacGillivray’s prion population on Gough is of utmost conservation relevance, as the relict macgillivrayi population in the Indian Ocean is very smallOpen Access funding enabled and organized by Projekt DEAL. PQ, JFM, TLC and LC were supported by the Deutsche Forschungsgemeinschaft (Germany), Heisenberg program (grant number DFG, Qu 148-5 to P.Q.). Logistical and financial support was obtained from the South African Department of Environmental Affairs, through the South African National Antarctic Programme. LDS was supported by a Rutherford Discovery Fellowship from the Royal Society of New ZealandWith the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)Peer reviewe

Introduced Mammalian Predators Induce Behavioural Changes in Parental Care in an Endemic New Zealand Bird

The introduction of predatory mammals to oceanic islands has led to the extinction of many endemic birds. Although introduced predators should favour changes that reduce predation risk in surviving bird species, the ability of island birds to respond to such novel changes remains unstudied. We tested whether novel predation risk imposed by introduced mammalian predators has altered the parental behaviour of the endemic New Zealand bellbird (Anthornis melanura). We examined parental behaviour of bellbirds at three woodland sites in New Zealand that differed in predation risk: 1) a mainland site with exotic predators present (high predation risk), 2) a mainland site with exotic predators experimentally removed (low risk recently) and, 3) an off-shore island where exotic predators were never introduced (low risk always). We also compared parental behaviour of bellbirds with two closely related Tasmanian honeyeaters (Phylidonyris spp.) that evolved with native nest predators (high risk always). Increased nest predation risk has been postulated to favour reduced parental activity, and we tested whether island bellbirds responded to variation in predation risk. We found that females spent more time on the nest per incubating bout with increased risk of predation, a strategy that minimised activity at the nest during incubation. Parental activity during the nestling period, measured as number of feeding visits/hr, also decreased with increasing nest predation risk across sites, and was lowest among the honeyeaters in Tasmania that evolved with native predators. These results demonstrate that some island birds are able to respond to increased risk of predation by novel predators in ways that appear adaptive. We suggest that conservation efforts may be more effective if they take advantage of the ability of island birds to respond to novel predators, especially when the elimination of exotic predators is not possible

endangered

Human-assisted spread of a maladaptive behavior in a criticall

Human-Assisted Spread of a Maladaptive Behavior in a Critically Endangered Bird

<div><p>Conservation management often focuses on counteracting the adverse effects of human activities on threatened populations. However, conservation measures may unintentionally relax selection by allowing the ‘survival of the not-so-fit’, increasing the risk of fixation of maladaptive traits. Here, we report such a case in the critically-endangered Chatham Island black robin (<i>Petroica traversi</i>) which, in 1980, was reduced to a single breeding pair. Following this bottleneck, some females were observed to lay eggs on the rims of their nests. Rim eggs left in place always failed to hatch. To expedite population recovery, rim eggs were repositioned inside nests, yielding viable hatchlings. Repositioning resulted in rapid growth of the black robin population, but by 1989 over 50% of all females were laying rim eggs. We used an exceptional, species-wide pedigree to consider both recessive and dominant models of inheritance over all plausible founder genotype combinations at a biallelic and possibly sex-linked locus. The pattern of rim laying is best fitted as an autosomal dominant Mendelian trait. Using a phenotype permutation test we could also reject the null hypothesis of non-heritability for this trait in favour of our best-fitting model of heritability. Data collected after intervention ceased shows that the frequency of rim laying has strongly declined, and that this trait is maladaptive. This episode yields an important lesson for conservation biology: fixation of maladaptive traits could render small threatened populations completely dependent on humans for reproduction, irreversibly compromising the long term viability of populations humanity seeks to conserve.</p></div

Fitness consequences of rim laying behavior.

<p>Data from 2007–11 (during which rim eggs were not repositioned) shows that females that laid rim eggs had a significantly reduced clutch size (i.e. number of eggs laid inside nests that were incubated), and decreased hatching and breeding success compared to normal-laying females. We obtain p-values from likelihood ratio tests with generalized linear mixed models of data with sample size <i>n</i>.</p

Inferred trajectories of allele A under the simple dominant model (model No. 4 in Table 2) between 1980 and 1989.

<p>The mean trajectory is shown by black line and the 50% and 95% confidence sets of the trajectories are shown in decreasing shades of grey. Twice the population size (total number of alleles) is shown by the dashed and dotted line.</p

Pedigree of all black robins breeding between 1980 and 1989.

<p>All individuals are labelled and descend from one breeding pair (A1 and A2). Males are shown as squares. Females that lay rim eggs are shown as red ircles and females that do not lay rim eggs are shown as blue circles (pedigree was generated using Pedigraph <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0079066#pone.0079066-Garbe1" target="_blank">[31]</a>).</p

Model Selection.

<p>Log likelihood and posterior probability of the phenotypes conditional on the pedigree, founder genotypes and model of inheritance. Z is a sex chromosome. The prior probability of each model is uniformly distributed and all other models considered (see text) have zero likelihood.</p

Landscape genomics: natural selection drives the evolution of mitogenome in penguins

Abstract Background Mitochondria play a key role in the balance of energy and heat production, and therefore the mitochondrial genome is under natural selection by environmental temperature and food availability, since starvation can generate more efficient coupling of energy production. However, selection over mitochondrial DNA (mtDNA) genes has usually been evaluated at the population level. We sequenced by NGS 12 mitogenomes and with four published genomes, assessed genetic variation in ten penguin species distributed from the equator to Antarctica. Signatures of selection of 13 mitochondrial protein-coding genes were evaluated by comparing among species within and among genera (Spheniscus, Pygoscelis, Eudyptula, Eudyptes and Aptenodytes). The genetic data were correlated with environmental data obtained through remote sensing (sea surface temperature [SST], chlorophyll levels [Chl] and a combination of SST and Chl [COM]) through the distribution of these species. Results We identified the complete mtDNA genomes of several penguin species, including ND6 and 8 tRNAs on the light strand and 12 protein coding genes, 14 tRNAs and two rRNAs positioned on the heavy strand. The highest diversity was found in NADH dehydrogenase genes and the lowest in COX genes. The lowest evolutionary divergence among species was between Humboldt (Spheniscus humboldti) and Galapagos (S. mendiculus) penguins (0.004), while the highest was observed between little penguin (Eudyptula minor) and Adélie penguin (Pygoscelis adeliae) (0.097). We identified a signature of purifying selection (Ka/Ks < 1) across the mitochondrial genome, which is consistent with the hypothesis that purifying selection is constraining mitogenome evolution to maintain Oxidative phosphorylation (OXPHOS) proteins and functionality. Pairwise species maximum-likelihood analyses of selection at codon sites suggest positive selection has occurred on ATP8 (Fixed-Effects Likelihood, FEL) and ND4 (Single Likelihood Ancestral Counting, SLAC) in all penguins. In contrast, COX1 had a signature of strong negative selection. ND4 Ka/Ks ratios were highly correlated with SST (Mantel, p-value: 0.0001; GLM, p-value: 0.00001) and thus may be related to climate adaptation throughout penguin speciation. Conclusions These results identify mtDNA candidate genes under selection which could be involved in broad-scale adaptations of penguins to their environment. Such knowledge may be particularly useful for developing predictive models of how these species may respond to severe climatic changes in the future

Identification of a Novel Adélie Penguin Circovirus at Cape Crozier (Ross Island, Antarctica).

Understanding the causes of disease in Antarctic wildlife is crucial, as many of these species are already threatened by environmental changes brought about by climate change. In recent years, Antarctic penguins have been showing signs of an unknown pathology: a feather disorder characterised by missing feathers, resulting in exposed skin. During the 2018-2019 austral summer breeding season at Cape Crozier colony on Ross Island, Antarctica, we observed for the first time an Adélie penguin chick missing down over most of its body. A guano sample was collected from the nest of the featherless chick, and using high-throughput sequencing, we identified a novel circovirus. Using abutting primers, we amplified the full genome, which we cloned and Sanger-sequenced to determine the complete genome of the circovirus. The Adélie penguin guano-associated circovirus genome shares &lt;67% genome-wide nucleotide identity with other circoviruses, representing a new species of circovirus; therefore, we named it penguin circovirus (PenCV). Using the same primer pair, we screened 25 previously collected cloacal swabs taken at Cape Crozier from known-age adult Adélie penguins during the 2014-2015 season, displaying no clinical signs of feather-loss disorder. Three of the 25 samples (12%) were positive for a PenCV, whose genome shared &gt;99% pairwise identity with the one identified in 2018-2019. This is the first report of a circovirus associated with a penguin species. This circovirus could be an etiological agent of the feather-loss disorder in Antarctic penguins