Evolution of correlated complexity in the radically different courtship signals of birds-of-paradise

This is the author accepted manuscript. The final version is available from Public Library of Science (PLoS) via the DOI in this record.Data accessibility: Data for primary analyses are included in S1 Data file.Ornaments used in courtship often vary wildly among species, reflecting the evolutionary interplay between mate preference functions and the constraints imposed by natural selection. Consequently, understanding the evolutionary dynamics responsible for ornament diversification has been a longstanding challenge in evolutionary biology. However, comparing radically different ornaments across species, as well as different classes of ornaments within species, is a profound challenge to understanding diversification of sexual signals. Using novel methods and a unique natural history dataset, we explore evolutionary patterns of ornament evolution in a group – the birds-of-paradise – exhibiting dramatic phenotypic diversification widely assumed to be driven by sexual selection. Rather than the trade-off between ornament types originally envisioned by Darwin and Wallace, we found positive correlations among cross-modal (visual/acoustic) signals indicating functional integration of ornamental traits into a composite unit – the courtship phenotype. Furthermore, given the broad theoretical and empirical support for the idea that systemic robustness – functional overlap and interdependency – promotes evolutionary innovation, we posit that birds-of-paradise have radiated extensively through ornamental phenotype space as a consequence of the robustness in the courtship phenotype that we document at a phylogenetic scale. We suggest that the degree of robustness in courtship phenotypes among taxa can provide new insights into the relative influence of sexual and natural selection on phenotypic radiations

Plumage Ornaments Signal Male Physiological Quality in Common Yellowthroats

Elaborate ornaments are thought to honestly signal quality to potential mates. These ornaments may signal a variety of physiological processes that affect health and fitness. I examined the relationship between ornaments and physiological quality in a bird, the common yellowthroat (Geothlypis trichas). Male common yellowthroats have two plumage ornaments, a black (eumelanin-based) mask and a yellow (carotenoid-based) bib. Males with larger masks are preferred by females for both extra-pair and social mates. I found that both the mask and the bib of male common yellowthroats honestly signal their ability to resist oxidative stress. Males with larger masks and more colorful bibs also produce a greater amount of corticosterone, a hormone that releases stored energy and induces adaptive behavioral changes, during a short-term stress response. This suggests that these ornaments signal how well males cope with stressful situations. In contrast, neither the mask or the bib signal the infection intensity of haemosporidian parasites across males in the population. However, haemosporidian infection intensity was not related to overwinter survival or body mass, suggesting that these parasites may not be very costly. Together, these results suggest that both melanin- and carotenoid-based plumage ornaments honestly signal male physiological quality in common yellowthroats

Differential deposition of antimicrobial proteins in blue tit (Cyanistes caeruleus) clutches by laying order and male attractiveness

Female birds can influence offspring fitness by varying the relative quantities of egg components they deposit within and between clutches. Antimicrobial proteins (lysozyme, ovotransferrin, and avidin) are significant components of the avian albumen and likely aid in defense of embryos from microbial infection. Within clutches, females may enhance antimicrobial defense of early-laid eggs to protect them from the high risk of infection incurred before the onset of incubation. Among entire clutches, females may invest more resources in young sired by more attractive males because they have higher reproductive value. We tested these hypotheses by quantifying antimicrobial protein distribution within and among clutches in blue tit eggs. Contrary to our hypothesis, clutches showed no differential deposition of lysozyme or avidin within clutches, but eggs laid in the middle of the sequence had higher concentrations of ovotransferrin than eggs in the beginning and end. Consistent with our second hypothesis, we found that females produced eggs with higher concentrations of lysozyme (although not ovotransferrin or avidin) when mated to more attractive (more UV-reflective) males. Furthermore, females mated to polygynous males deposited less lysozyme than those mated to monogamous males. These data suggest that allocation of lysozyme at the clutch level may be a maternal effect mediated by male qualities

Animal coloration patterns: linking spatial vision to quantitative analysis

Animal coloration patterns, from zebra stripes to bird egg speckles, are remarkably varied. With research on the perception, function, and evolution of animal patterns growing rapidly, we require a convenient framework for quantifying their diversity, particularly in the contexts of camouflage, mimicry, mate choice, and individual recognition. Ideally, patterns should be defined by their locations in a low-dimensional pattern space that represents their appearance to their natural receivers, much as color is represented by color spaces. This synthesis explores the extent to which animal patterns, like colors, can be described by a few perceptual dimensions in a pattern space. We begin by reviewing biological spatial vision, focusing on early stages during which neurons act as spatial filters or detect simple features such as edges. We show how two methods from computational vision—spatial filtering and feature detection—offer qualitatively distinct measures of animal coloration patterns. Spatial filters provide a measure of the image statistics, captured by the spatial frequency power spectrum. Image statistics give a robust but incomplete representation of the appearance of patterns, whereas feature detectors are essential for sensing and recognizing physical objects, such as distinctive markings and animal bodies. Finally, we discuss how pattern space analyses can lead to new insights into signal design and macroevolution of animal phenotypes. Overall, pattern spaces open up new possibilities for exploring how receiver vision may shape the evolution of animal pattern signals

New horizons for female birdsong : evolution, culture and analysis tools : a thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Ecology at Massey University, Auckland, New Zealand

Published papers appear in Appendix 7.1. and 7.2 respectively under a CC BY 4.0 and CC BY licence: Webb, W. H., Brunton, D. H., Aguirre, J. D., Thomas, D. B., Valcu, M., & Dale, J. (2016). Female song occurs in songbirds with more elaborate female coloration and reduced sexual dichromatism. Frontiers in Ecology and Evolution, 4(22). https://doi.org/10.3389/fevo.2016.00022 Yukio Fukuzawa, Wesley Webb, Matthew Pawley, Michelle Roper, Stephen Marsland, Dianne Brunton, & Andrew Gilman. (2020). Koe: Web-based software to classify acoustic units and analyse sequence structure in animal vocalisations. Methods in Ecology and Evolution, 11(3). https://doi.org/10.1111/2041-210X.13336As a result of male-centric, northern-hemisphere-biased sexual selection theory, elaborate female traits in songbirds have been largely overlooked as unusual or non-functional by-products of male evolution. However, recent research has revealed that female song is present in most surveyed songbirds and was in fact the ancestral condition to the clade. Additionally, a high proportion of songbird species have colourful females, and both song and showy colours have demonstrated female-specific functions in a growing number of species. We have much to learn about the evolution and functions of elaborate female traits in general, and female song in particular. This thesis extends the horizons of female birdsong research in three ways: (1) by revealing the broad-scale evolutionary relationship of female song and plumage elaboration across the songbirds, (2) by developing new accessible tools for the measurement and analysis of song complexity, and (3) by showing—through a detailed field study on a large natural metapopulation—how vocal culture operates differentially in males and females. First, to understand the drivers of elaborate female traits, I tested the evolutionary relationship between female song presence and plumage colouration across the songbirds. I found strong support for a positive evolutionary correlation between traits, with female song more prevalent amongst species with elaborated female plumage. These results suggest that contrary to the idea of trade-off between showy traits, female plumage colouration and female song likely evolved together under similar selection pressures and that their respective functions are reinforcing. Second, I introduce new bioacoustics software, Koe, designed to meet the need for detailed classification and analysis of song complexity. The program enables visualisation, segmentation, rapid classification and analysis of song structure. I demonstrate Koe with a case study of New Zealand bellbird Anthornis melanura song, showcasing the capabilities for large-scale bioacoustics research and its application to female song. Third, I conducted one of the first detailed field-based analyses of female song culture, studying an archipelago metapopulation of New Zealand bellbirds. Comparing between male and female sectors of each population, I found equal syllable diversity, largely separate repertoires, and contrasting patterns of sharing between sites—revealing female dialects and pronounced sex differences in cultural evolution. By combining broad-scale evolutionary approaches, novel song analysis tools, and a detailed field study, this thesis demonstrates that female song can be as much an elaborate signal as male song. I describe how future work can build on these findings to expand understanding of elaborate female traits

COLOURATION AS AN INTRASPECIFIC SIGNAL IN BIRDS

Colour variation seems to be a pivotal trait in avian communication dynamics, where information is provided to recipients by \u2018signallers\u2019 through colouration. Plumage colours can be structural or due to pigments incorporated into the keratin of feathers, and melanin-based colouration, produced by the melanocortin system, is one of the most common in birds. Melanin-based colouration is under genetic control and the degree of melanism is often associated with variation in physiological, behavioural and life-history traits, due to pleiotropic effects of the compounds regulating the melanin synthesis. However, variability in colouration is observed not only among plumage traits but also in fleshy ornaments, legs or eggshells. Variation in eggshell pigmentation, determined by biliverdin and protoporphyrin pigments, may accomplish several different functions, the most obvious of which are camouflage and background matching. It has been also proposed that intra-specific variation in eggshell pigmentation patterns could reflect egg, maternal or paternal traits and hence provides reliable cues to conspecifics about egg, maternal or paternal quality. The first part of the studies presented in this thesis is aimed at investigating the role of melanin-based colouration from different points of view. I started by investigating the role of melanin-based colouration in barn swallow nestling (Hirundo rustica) as a signal of individual quality and its covariation with behavioural stress response. Moreover, I investigated the covariation of genes regulating melanin-based plumage colouration and plumage polymorphism in lesser kestrel males (Falco naumanni). Secondly, since the relationship between protoporphyrin-based eggshell pigmentation and egg or maternal/paternal traits appears to be highly variable among species, I investigated the possible signalling role of protoporphyrin-based eggshell pigmentation in both study species. Using both experimental and correlative approaches, I found that even if pleiotropic effects of melanocortin system may still drive the associations between melanin-based colouration and individual quality, the melanocortin pleiotropic hypothesis may not apply to plumage colouration deriving from mixing of eu- and pheomelanins. Moreover, results on the potential signalling role of protoporphyrin-based eggshell pigmentation in two distantly related bird species support the idea that intraspecific signalling via eggshell pigmentation is species-specific feature rather than a general pattern among avian taxa

Population Dynamics and Management Implications for American White Pelicans (Pelecanus Erythrorhynchos) Breeding at Marsh Lake, Lac Qui Parle Wildlife Management Area, Minnesota

The American white pelican (Pelecanus erythrorhynchos) is a prominent breeding bird in Minnesota, but little information has been available on their production, population dynamics, growth and development, or demographic characteristics. I examined life-history traits of American white pelicans nesting colonially at Marsh Lake, Lac qui Parle Wildlife Management Area, Minnesota. Marsh Lake is an impounded river floodplain lake on the Upper Minnesota River that holds the largest American white pelican breeding colony in Minnesota (and one of the largest American white pelican breeding colonies in North America). An analysis of colony population levels and spring streamflow data indicated that more than 84% of the variation in the number of near-fledged chicks produced per nest was related to mean daily discharge during April. In years when high water floods preferred low-elevation nesting habitat on islands in the middle of the lake, American white pelicans are forced to establish nests on high-elevation sites that are closer to the mainland. The proximity to the mainland leaves the high-elevation sites accessible to mainland mammalian predators, and production rates decline. An examination of size at hatch and growth of American white pelican chicks showed little variation in initial size and growth rates between years. However, substantial variation in initial size and growth rates were detected within season depending on the timing of hatch. Initial mass did not vary throughout the nesting season, but initial tarsus and wing length were shorter in chicks hatched later in the season. However, growth rates for mass, tarsus, and wing were faster for late-hatched chicks, potentially allowing late-hatched chicks to fledge at an earlier age. An analysis of demographic characteristics of American white pelicans nesting at Marsh Lake indicated timing of nest initiation was not related to age or body condition of adults. However, nests were initiated earlier on the preferred nesting island at Marsh Lake. Although some individuals may nest at an earlier age, the estimated age of maturation for American white pelicans nesting at Marsh Lake suggests they are unlikely to begin nesting until they are at least five years old

Hybrid Zone Dynamics Between Saltmarsh (Ammodramus caudacutus) and Nelson\u27s (Ammodramus nelsoni) Sparrows

Hybrid zones in nature have long been equated to “windows on the evolutionary process” providing unique environments to understand patterns of gene flow and introgression and the role of these mechanisms in maintaining biodiversity. Ongoing hybridization and introgression can lead to a number of conservation and evolutionary outcomes; as such, identifying the role of introgression in natural populations can provide new insights into species interactions while contributing to our understanding of evolutionary theory. The research presented below characterizes hybrid zone dynamics between two tidal marsh endemics – the Saltmarsh (Ammodramus caudacutus) and Nelson’s (Ammodramus nelsoni) sparrow. Both species co-inhabit salt marshes from southern Maine to northern Massachusetts and hybridization has been documented in the overlap zone for over a century. While there is previous evidence for asymmetrical introgression and southward expansion, information regarding the rates and consequences of hybridization in this system is lacking. To address this objective, I evaluated five components that define a hybrid zone: 1) phenotypic and morphological variation; 2) strength of selection and patterns of introgression; 3) influence of habitat; 4) hybrid fitness; and 5) temporal stability. I combined genetic and ecological methods to evaluate the above components and to assess hybrid zone dynamics. I collected morphometric and plumage data from individuals sampled extensively across the hybrid zone and evaluated both phenotypic and genetic variation in pure and admixed populations. I found that morphological and genetic variation increased in sympatric populations and that a majority of the individuals sampled were backcrossed with a lack of both intermediate phenotypes and genotypes. I also found that plumage traits related to the darkness and definition of streaking on the breast, flanks, and back of the birds correlated more strongly with genotype than traits related to the amount of streaking on an individual or the color of the plumage. I also investigated patterns of genetic structure, selection, and differential introgression across the hybrid zone. I found that a high proportion (50%) of the sampled individuals were admixed to some degree, but that only 3% of individuals were recent generation hybrids. Genetic analyses revealed that pure and hybrid individuals were patchily distributed across the hybrid zone. I also found that introgression was highly variable among marker types and that, for a majority of the markers examined, selection was weak and introgression was asymmetrical toward Saltmarsh Sparrows. I did document abrupt patterns of selection for sex-linked markers, mitochondrial markers, and two gene-associated markers. Selection for sex-linked and mitochondrial markers supports findings of Haldane’s rule in this system. These results suggest a role for selection in maintaining pure species boundaries in the face of ongoing geneflow and introgression. I also investigated patterns of genetic structure, selection, and differential introgression across the hybrid zone. I found that a high proportion (50%) of the sampled individuals were admixed to some degree, but that only 3% of individuals were recent generation hybrids. Genetic analyses revealed that pure and hybrid individuals were patchily distributed across the hybrid zone. I also found that introgression was highly variable among marker types and that, for a majority of the markers examined, selection was weak and introgression was asymmetrical toward Saltmarsh Sparrows. I did document abrupt patterns of selection for sex-linked markers, mitochondrial markers, and two gene-associated markers. Selection for sex-linked and mitochondrial markers supports findings of Haldane’s rule in this system. These results suggest a role for selection in maintaining pure species boundaries in the face of ongoing geneflow and introgression. To identify patterns of differential fitness across the hybrid zone, I compared numerous reproductive parameters among pure, backcrossed, and recent generation hybrid females. I also compared the proportion of first generation hybrids among age and gender classes to test for differences in survival in hybrids. I found that pure and backcrossed Nelson’s Sparrows have reduced hatching and fledgling success compared to hybrids and pure and backcrossed Saltmarsh Sparrows. The reduced fitness in Nelson’s Sparrows is likely due to differential adaptation to coastal marshes and may be influential in shaping hybrid zone dynamics and asymmetries in this system. Also, hybrid females had lower survival than hybrid males. Lastly, I evaluated temporal stability in the hybrid zone by comparing genetic and morphological data between two temporal replicates. I compared plumage data, morphometric measurements, and data from neutral and mitochondrial markers between five marshes sampled in 1998 and then again 15 years later in 2012/2013. I detected a southward expansion of Nelson’s Sparrow alleles, supported by a shift in the center of the hybrid zone and an increase in introgression over the 15-year time period. Despite signs of hybrid zone expansion, some markers are under stronger selection now than they were in 1998 indicating that some genetic regions may be maintained despite introgression. These regions may be critical in maintaining species boundaries. Following the assumptions of existing theoretical frameworks, the above components were systematically evaluated to assess hybrid zone stability. The data have been used to evaluate impacts of hybridization and introgression in a naturally occurring avian hybrid zone. The work presented here identifies the mechanisms responsible for maintaining pure species boundaries in the face of ongoing introgression and gene flow. Further, this work has elucidated how hybridization shapes population dynamics while providing insight into the conservation management of hybridizing species. Although hybridization is ongoing between the two species, selective mechanisms likely play a role in reproductive isolation. Based on these findings, the management of both species, even within the hybrid zone, is warranted. This insight is particularly relevant to the management of Saltmarsh Sparrows, as this species is imminently threatened by habitat loss through sea level rise and the management and conservation of genetically “pure” populations is a high priority in the northeast

What is it vs Who did it? A review of the lack of human focused forensic evidence in the context of wildlife crime

Wildlife crime suffers from low prosecution and conviction rates, with a lack of evidence and resources cited as hurdles to enforcement. Forensic evidence is used in human-on-human crimes to identify perpetrators and link individuals to criminal activity. Forensics approaches in the context of wildlife crime are heavily focused on non-human evidence using DNA barcoding to establish species and geographical origins. In human-on-human crime fingermarks and DNA profiling are two of the most recognisable forensic evidence types, both with significant global infrastructure, which contribute to prosecutions and convictions. Wildlife products can be the only physical evidence type available in a wildlife crime but attempts to recover human forensic evidence from them is a relatively unexplored area. The research that does exist demonstrates fingermark and touch DNA evidence can be collected in many contexts from several different species. Despite this there has been only one report of utilisation of this type human evidence recovery in wildlife case work. Failure to consider all potential evidence types has a negative impact on wildlife crime investigations. There is a need to experimentally assess the benefits and limitations associated with the collection of human evidence from wildlife items. This article introduces key factors that affect the recovery of human fingermarks and touch DNA evidence before focussing on the limited number of instances where these methods have been applied to wildlife forensic research and what considerations should be taken when developing further work in this field