The Shapes of Birds' Eggs: Evolutionary Constraints and Adaptations.

AbstractWe studied the shapes of eggs from 955 extant bird species across the avian phylogeny, including 39 of 40 orders and 78% of 249 families. We show that the elongation component of egg shape (length relative to width) is largely the result of constraints imposed by the female's anatomy during egg formation, whereas asymmetry (pointedness) is mainly an adaptation to conditions during the incubation period. Thus, egg elongation is associated with the size of the egg in relation to both the size of the female's oviduct and her general body conformation and mode of locomotion correlated with pelvis shape. Egg asymmetry is related mainly to clutch size and the structure of the incubation site, factors that influence thermal efficiency during incubation and the risk of breakage. Importantly, general patterns across the avian phylogeny do not always reflect the trends within lower taxonomic levels. We argue that the analysis of avian egg shape is most profitably conducted within taxa where all species share similar life histories and ecologies, as there is no single factor that influences egg shape in the same way in all bird species.

Three decades of sperm competition in birds.

In the three decades, since Birkhead and Møller published Sperm competition in birds (1992, Academic Press) more than 1000 papers have been published on this topic, about half of these being empirical studies focused on extrapair paternity. Both technological innovations and theory have moved the field forward by facilitating the study of both the mechanisms underlying sperm competition in both sexes, and the ensuing behavioural and morphological adaptations. The proliferation of studies has been driven partly by the diversity of both behaviours and morphologies in birds that have been influenced by sperm competition, but also by the richness of the theory developed by Geoff Parker over the past 50 years. This article is part of the theme issue 'Fifty years of sperm competition'.

Accurately quantifying the shape of birds' eggs.

Describing the range of avian egg shapes quantitatively has long been recognized as difficult. A variety of approaches has been adopted, some of which aim to capture the shape accurately and some to provide intelligible indices of shape. The objectives here are to show that a (four-parameter) method proposed by Preston (1953, The Auk, 70, 160) is the best option for quantifying egg shape, to provide and document an R program for applying this method to suitable photographs of eggs, to illustrate that intelligible shape indices can be derived from the summary this method provides, to review shape indices that have been proposed, and to report on the errors introduced using photographs of eggs at rest rather than horizontal.

A trade-off between thickness and length in the zebra finch sperm mid-piece.

The sperm mid-piece has traditionally been considered to be the engine that powers sperm. Larger mid-pieces have therefore been assumed to provide greater energetic capacity. However, in the zebra finch Taeniopygia guttata, a recent study showed a surprising negative relationship between mid-piece length and sperm energy content. Using a multi-dimensional approach to study mid-piece structure, we tested whether this unexpected relationship can be explained by a trade-off between mid-piece length and mid-piece thickness and/or cristae density inside the mitochondrial helix. We used selective plane illumination microscopy to study mid-piece structure from three-dimensional images of zebra finch sperm and used high-resolution transmission electron microscopy to quantify mitochondrial density. Contrary to the assumption that longer mid-pieces are larger and therefore produce or contain a greater amount of energy, our results indicate that the amount of mitochondrial material is consistent across mid-pieces of varying lengths, and longer mid-pieces are simply proportionately 'thinner'.

A sex-linked supergene controls sperm morphology and swimming speed in a songbird.

Sperm competition is an important selective force in many organisms. As a result, sperm have evolved to be among the most diverse cells in the animal kingdom. However, the relationship between sperm morphology, sperm motility and fertilization success is only partially understood. The extent to which between-male variation is heritable is largely unknown, and remarkably few studies have investigated the genetic architecture of sperm traits, especially sperm morphology. Here we use high-density genotyping and gene expression profiling to explore the considerable sperm trait variation that exists in the zebra finch Taeniopygia guttata. We show that nearly all of the genetic variation in sperm morphology is caused by an inversion polymorphism on the Z chromosome acting as a 'supergene'. These results provide a striking example of two evolutionary genetic predictions. First, that in species where females are the heterogametic sex, genetic variation affecting sexually dimorphic traits will accumulate on the Z chromosome. Second, recombination suppression at the inversion allows beneficial dominant alleles to become fixed on whichever haplotype they first arise, without being exchanged onto other haplotypes. Finally, we show that the inversion polymorphism will be stably maintained by heterozygote advantage, because heterozygous males have the fastest and most successful sperm.

Allopreening in birds is associated with parental cooperation over offspring care and stable pair bonds across years.

Individuals of many species form bonds with their breeding partners, yet the mechanisms maintaining these bonds are poorly understood. In birds, allopreening is a conspicuous feature of interactions between breeding partners and has been hypothesized to play a role in strengthening and maintaining pair bonds within and across breeding attempts. Many avian species, however, do not allopreen and the relationship between allopreening and pair bonding across species remains unexplored. In a comparative analysis of allopreening and pair bond behavior, we found that allopreening between breeding partners was more common among species where parents cooperate to rear offspring. The occurrence of allopreening was also associated with an increased likelihood that partners would remain together over successive breeding seasons. However, there was no strong evidence for an association between allopreening and sexual fidelity within seasons or time spent together outside the breeding season. Allopreening between partners was also no more common in colonial or cooperatively breeding species than in solitary species. Analyses of evolutionary transitions indicated that allopreening evolved from an ancestral state of either high parental cooperation or high partner retention, and we discuss possible explanations for this. Overall, our results are consistent with an important role for allopreening in the maintenance of avian pair bonds.

Red Carotenoid Coloration in the Zebra Finch Is Controlled by a Cytochrome P450 Gene Cluster.

Bright-red colors in vertebrates are commonly involved in sexual, social, and interspecific signaling [1-8] and are largely produced by ketocarotenoid pigments. In land birds, ketocarotenoids such as astaxanthin are usually metabolically derived via ketolation of dietary yellow carotenoids [9, 10]. However, the molecular basis of this gene-environment mechanism has remained obscure. Here we use the yellowbeak mutation in the zebra finch (Taeniopygia guttata) to investigate the genetic basis of red coloration. Wild-type ketocarotenoids were absent in the beak and tarsus of yellowbeak birds. The yellowbeak mutation mapped to chromosome 8, close to a cluster of cytochrome P450 loci (CYP2J2-like) that are candidates for carotenoid ketolases. The wild-type zebra finch genome was found to have three intact genes in this cluster: CYP2J19A, CYP2J19B, and CYP2J40. In yellowbeak, there are multiple mutations: loss of a complete CYP2J19 gene, a modified remaining CYP2J19 gene (CYP2J19(yb)), and a non-synonymous SNP in CYP2J40. In wild-type birds, CYP2J19 loci are expressed in ketocarotenoid-containing tissues: CYP2J19A only in the retina and CYP2J19B in the beak and tarsus and to a variable extent in the retina. In contrast, expression of CYP2J19(yb) is barely detectable in the beak of yellowbeak birds. CYP2J40 has broad tissue expression and shows no differences between wild-type and yellowbeak. Our results indicate that CYP2J19 genes are strong candidates for the carotenoid ketolase and imply that ketolation occurs in the integument in zebra finches. Since cytochrome P450 enzymes include key detoxification enzymes, our results raise the intriguing possibility that red coloration may be an honest signal of detoxification ability.