Theory of the growth and evolution of feather shape

We present the first explicit theory of the growth of feather shape, defined as the outline of a pennaceous feather vane. Based on a reanalysis of data from the literature, we propose that the absolute growth rate of the barbs and rachis ridges, not the vertical growth rate, is uniform throughout the follicle. The growth of feathers is simulated with a mathematical model based on six growth parameters: (1) absolute barb and rachis ridge growth rate, (2) angle of helical growth of barb ridges, (3) initial barb ridge number, (4) new barb ridge addition rate, (5) barb ridge diameter, and (6) the angle of barb ramus expansion following emergence from the sheath. The model simulates growth by cell division in the follicle collar and, except for the sixth parameter, does not account for growth by differentiation in cell size and shape during later keratinization. The model can simulate a diversity of feather shapes that correspond closely in shape to real feathers, including various contour feathers, asymmetrical feathers, and even emarginate primaries. Simulations of feather growth under different parameter values demonstrate that each parameter can have substantial, independent effects on feather shape. Many parameters also have complex and redundant effects on feather shape through their influence on the diameter of the follicle, the barb ridge fusion rate, and the internodal distance. Simulated isochrones-the loci, or sets, of feather cells of the same age-have the same oblique chevron-shaped position in the mature feather as fault bars, which are isochronic defects in the barbules created by a disruptions during development. Accurate simulation of fault bar shape and position confirms the uniform absolute growth rate hypothesis and the general realism of the model. The theory defines a six-parameter feather morphospace, and provides many predictions about the developmental determination of feather shape that can be tested with detailed observations and experiments on developing feathers. This theory also provides testable predictions about the changes in developmental mechanisms required to evolve different feather shapes to accomplish various functions.     

Losing the last feather: feather loss as an antipredator adaptation in birds

Birds often lose feathers during predation attempts, and thisability has evolved as a means of escape. Because predatorsare more likely to grab feathers on the rump and the back thanon the ventral side of an escaping bird, we predicted that theformer feathers would have evolved to be relatively looselyattached as an antipredator strategy in species that frequentlydie from predation. We estimated the force required to removefeathers from the rump, back, and breast by pulling featherswith a spring balance from a range of European bird speciesin an attempt to investigate ecological factors associated withease of feather loss during predation attempts. The force requiredto loosen a feather from the rump was less than that requiredto loosen a feather from back, which in turn was less than thatrequired to loosen a feather from the breast. The relative forceneeded to loosen rump feathers compared with feathers from theback and the breast was smaller for prey species preferred bythe most common predator of small passerine birds, the sparrowhawkAccipiter nisus. Likewise, the relative force was also smallerin species with a high frequency of complete tail loss amongfree-living birds, which we used as an index of the frequencyof failed predation attempts. The relative force required toremove feathers from the rump was smaller in species with ahigh frequency of fear screams, another measure of the relativeimportance of predation as a cause of death. Feather loss requiredparticularly little force among solitarily breeding bird speciesthat suffer the highest degree of predation. Antipredator defensein terms of force required to remove feathers from the rumpwas larger in species with a strong antiparasite defense interms of T-cell–mediated immune response. These findingsare consistent with the hypothesis that different defenses areantagonistic and that they are traded off against each other.     

Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape.

The cytoplasmic tails of the influenza virus glycoproteins hemagglutinin (HA) and neuraminidase (NA) are highly conserved in sequence for all virus subtypes and it is believed that assembly of this enveloped virus depends on interactions of these domains with cytoplasmic viral components. However, it is possible to rescue altered influenza viruses lacking either the HA or NA cytoplasmic tails. We have obtained an influenza virus that lacks both the cytoplasmic tail of HA and NA. Particle production is reduced approximately 10-fold but these particles, although having a fairly normal protein composition, are greatly elongated and of extended irregular shape. We propose a model in which the interactions of the cytoplasmic tails of HA and NA with an internal viral component are so important for spherical virion shape that there is dual redundancy in the interactions.     

Why some rails have white tails: the evolution of white undertail plumage and anti-predator signaling

Conspicuous plumage patches have evolved in birds as conspecific signals for mate attraction and assessment, intersexual competition or to signal alarm. Signals may alternatively be directed at potential predators to discourage pursuit. Rails (Family Rallidae) are ground-dwelling birds, many of which inhabit wetlands, while others occur in forests and grasslands. They are renown for their secretive nature and the tendency to flick their tails when observed. This behavior is more conspicuous in species with white undertail coverts that contrast sharply with darker body plumage. Using species comparisons and controlling for phylogeny, we investigated four hypotheses for the evolution of white undertail coverts in rails. We found little support for the hypothesis that white tails are sexually selected: white tails were not more common in species with polygamous as opposed to monogamous mating systems, species with sexual dimorphism, nor species that display their tails in courtship. Nor did our results support the hypothesis that white tail plumage evolved for intersexual competition during territorial interactions. Instead, we found that species that flock for at least part of the year and species found in open as opposed to concealing habitats were significantly more likely to have white undertail coverts. Rail species inhabiting concealing habitats are less commonly gregarious and more likely selected for crypsis. Using phylogenetically-controlled statistical inference we found that adaptation to open wetland habitats significantly precedes the evolution of white undertails, whereas gregariousness likely evolved later in some lineages. The inferred order of trait evolution suggests that this plumage characteristic could have been selected primarily for enhancement of an anti-predator signal rather than a social signal for conspecifics.     

Evolution of pistil length as a choice mechanism for pollen quality

During the fertilisation process in plants, pollen tube growth rate may be selected as a trait important in male to male competition. Since female morphology provides the necessary selective arena for such competition, we investigate if sexual selection theory can be used to explain the evolution of pistil length as a female choice mechanism. This choice is performed by direct interference with male to male competition. Furthermore, the sessile nature of plants limits the number of mates a female can choose between, which could limit the benefit a female can gain from distinguishing between donors. To mirror these circumstances, we model a situation when there are only two competitors at a time. Using a game theoretical approach we show that if pollen tube growth rate can be used as an indication of heritable quality, pistil length can be selected in response to variation of this trait. We further find that length of the pistil affects selection of pollen tube growth rate. Thus female preference and male competitive ability co-evolve, but this does not necessarily lead to a positive relationship between the two. Under certain circumstances we find a negative relation instead. Given realistic differences in male quality, the model indicates that there is a potential for evolution of female morphology as a choice mechanism for pollen quality.     

Concealed by conspicuousness: distractive prey markings and backgrounds

High-contrast markings, called distractive or dazzle markings, have been suggested to draw and hold the attention of a viewer, thus hindering detection or recognition of revealing prey characteristics, such as the body outline. We tested this hypothesis in a predation experiment with blue tits (Cyanistes caeruleus) and artificial prey. We also tested whether this idea can be extrapolated to the background appearance and whether high-contrast markings in the background would improve prey concealment. We compared search times for a high-contrast range prey (HC-P) and a low-contrast range prey (LC-P) in a high-contrast range background (HC-B) and a low-contrast range background (LC-B). The HC-P was more difficult to detect in both backgrounds, although it did not match the LC-B. Also, both prey types were more difficult to find in the HC-B than in the LC-B, in spite of the mismatch of the LC-P. In addition, the HC-P was more difficult to detect, in both backgrounds, when compared with a generalist prey, not mismatching either background. Thus, we conclude that distractive prey pattern markings and selection of microhabitats with distractive features may provide an effective way to improve camouflage. Importantly, high-contrast markings, both as part of the prey coloration and in the background, can indeed increase prey concealment.     

Sperm length and quality in sperm-dependent parthenogens

Is the male function of parthenogenetic hermaphrodites a historic remnant or an adaptive investment? In the first case, one would expect the male function to be ‘degraded’ and, in the second case, fully functional, despite being reduced. To answer this question, we investigated sperm morphology and quality in the hermaphroditic planarian Schmidtea polychroa. Parthenogenetic forms of this species are sperm‐dependent and require allosperm to trigger embryogenesis. Although there is generally no genetic paternal contribution, occasional fertilization of parthenogenetic eggs has been reported, leading to genetic changes in an otherwise apomictic lineage (‘occasional sex’). Comparing two locations, one with pure clonality and one with occasional sexuality, revealed substantial differences in both sperm length and fertility: Occasional sex appears to be coupled with longer sperm and higher sperm quality. We discuss the implications of these results for the maintenance of the male function in sperm‐dependent parthenogens. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93 , 81–87.     

The making of a feather: Homeoproteins,retinoids and adhesion molecules

We have been using feather development as a model for understanding the molecular basis of pattern formation and to explore the roles of homeoproteins, retinoids and adhesion molecules in this process. Two kinds of homeobox (Hox) protein gradients in the skin have been identified: a ‘microgradient’ within a single feather bud and a ‘macrogradient’ across the feather tract. The asynchronous alignment of different Hox macrogradients establishes a unique repertoire of Hox expression patterns in skin appendages within the integument, designated here as the ‘Hox codes of skin appendages’. It is hypothesized that these Hox codes contribute to the phenotypic determination of skin appendages. High doses of retinoic acid cause a morphological transformation between feather and scale, while low doses of retinoic acid cause an alteration of the axial orientation of skin appendages. We have tested the ability of molecules directly involved in the feather formation process to mediate the action of the Hox codes, and surmise that adhesion molecules are potential candidates. Using specific Fabs to suppress the activity of adhesion molecules, we have found that L-CAM is involved in the formation of the hexagonal pattern, N-CAM is involved in mediating dermal condensations, tenascin is involved in feather bud growth and elongation, and integrin β-1 is essential for epithelial-mesenchymal interactions. More work is in progress to fully understand the molecular pathways regulating the feather formation process.     

Sexual displays as amplifiers: practical examples with an emphasis on feather decorations

Exact patterns of displays are not easy to explain on a functionalbasis. However, if displays evolve initially as amplifiers ofpreviously perceived differences in quality, their patternsshould correspond with patterns of quality cues that are amplified.Consequently, exact patterns of behavioral, morphological, andstructural displays can be explained. I illustrate this withexamples of some feather decorations. Furthermore, these examplesindicate that, frequently, cues on which female choice is basedcannot easily run away, whereas their amplifiers can. Finally,I present specific predictions of the amplifying theory of sexualselection.     

Increase of feather quality during moult: a possible implication of feather deformities in the evolution of partial moult in the great tit Parus major

Here we investigate the change in feather quality during partial post‐juvenile and complete post‐breeding moult in great tit Parus major by measuring the change in the number of fault bars and feather holes on wing and tail feathers. Feathers grown during ontogeny usually are of lower quality than feathers grown following subsequent moults at independence. This is reflected by higher number of fault bars and feather holes on juveniles compared to adults. Fault bars are significantly more common on tail and proximal wing feathers than on the distal remiges, indicating a mechanism of adaptive allocation of stress induced abnormalities during ontogeny into the aerodynamically less important flight feathers. On the contrary, feather holes produced probably by chewing lice have a more uniform distribution on wing and tail feathers, which may reflect the inability of birds to control their distribution, or the weak natural selection imposed by them. The adaptive value of the differential allocation of fault bar between groups of feathers seems to be supported by the significantly higher recapture probability of those juvenile great tits which have fewer fault bars at fledging on the aerodynamically most important primaries, but not on other groups of flight feathers. The selection imposed by feather holes seems to be smaller, since except for the positive association between hatching date, brood size and the number of feather holes at fledging, great tits' survival was not affected by the number of feather holes. During post‐juvenile moult, the intensity of fault bars drops significantly through the replacement of tail feathers and tertials, resulting in disproportional reduction of the total number of fault bars on flight feathers related to the number of feathers replaced. The reduction in the number of fault bars during post‐juvenile moult associated with their adaptive allocation to proximal wing feathers and rectrices may explain the evolution of partial post‐juvenile moult in the great tit, since the quality of flight feathers can be increased significantly at a relatively small cost. Our results may explain the widespread phenomenon of partial post‐juvenile moult of flight feathers among Palearctic passerines. During the next complete post‐breeding moult, the total number of fault bars on flight feathers has remained unchanged, indicating the effectiveness of partial post‐juvenile moult in reducing the number of adaptively allocated fault bars. The number of feather holes has also decreased on groups of feathers replaced during partial post‐juvenile moult, but the reduction is proportional with the number of feathers moulted. In line with this observation, the number of feather holes is further reduced during post‐breeding moult on primaries and secondaries, resulting in an increase in feather quality of adult great tits.     

Tail length in birds in relation to tail shape,general flight ecology and sexual selection

Relative tail length (longtailedness) of Palearctic birds was assessed by the standardized residuals of log–log regressions of tail length on wing length and tarsus length. The mean degree of tail shortening was greater than mean degree of tail lengthening, but there was a greater frequency of extreme long-tailed than short-tailed species. Longtailedness was greater in ornamental pin, lyre, deep forked and graduated shaped tails. These shapes (except graduated, for which data were lacking) were also relatively long-tailed according to shortest-rectrix lengths, this extra length potentially contributing compensatory lift. In forked tails, tail ratio increased linearly with longtailedness to above the aerodynamic optimum, and thus the most elongated forked tails were also more deeply forked. Tail shortening was marked for rounded tails, a surprising result in view of their slightly ornamental shape. Phylogenetically independent contrasts showed significantly greater longtailedness in graduated than square-tailed species, confirming the species-wide analysis. In phylogenetically independent contrasts of longtailedness and ecological factors, short-tailed species had significantly greater flight distances than medium-tailed species, but long- and medium-tailed species did not differ in migratory distance, foraging distance, overall flight distance or importance of aerial foraging. The data suggest that ecological factors, i.e. natural selection, are more important in the evolution of short-tailedness than longtailedness in birds, and that an additional influence of sexual selection on tail length and shape is also widespread.     

Functional overlap and regulatory links shape genetic interactions between signaling pathways

To understand relationships between phosphorylation-based signaling pathways, we analyzed 150 deletion mutants of protein kinases and phosphatases in S. cerevisiae using DNA microarrays. Downstream changes in gene expression were treated as a phenotypic readout. Double mutants with synthetic genetic interactions were included to investigate genetic buffering relationships such as redundancy. Three types of genetic buffering relationships are identified: mixed epistasis, complete redundancy, and quantitative redundancy. In mixed epistasis, the most common buffering relationship, different gene sets respond in different epistatic ways. Mixed epistasis arises from pairs of regulators that have only partial overlap in function and that are coupled by additional regulatory links such as repression of one by the other. Such regulatory modules confer the ability to control different combinations of processes depending on condition or context. These properties likely contribute to the evolutionary maintenance of paralogs and indicate a way in which signaling pathways connect for multiprocess control.     

Potential for control of signaling pathways via cell size and shape

BACKGROUND: In order for signals generated at the plasma membrane to reach intracellular targets, activated messengers, such as G proteins and phosphoproteins, must diffuse through the cytoplasm. If the deactivators of these messengers, GTPase activating proteins (GAPs) and phosphatases, respectively, are sufficiently active in the cytoplasm, then the signal could in principle decay before reaching the target and a stable spatial gradient in phosphostate would be generated. Recent experiments document the existence of such gradients in living cells and suggest a role for them in mitotic spindle morphogenesis and cell migration. However, how such systems behave theoretically when embedded in a cell of varying size or shape has not been considered. RESULTS: Here we use a simple mathematical model to explore the theoretical consequences of a plasma membrane bound activator (i.e., guanine nucleotide exchange factor, GEF, or kinase) and a cytoplasmic deactivator (i.e., GAP or phosphatase), and we find that as a model cell grows, the substrate becomes progressively dephosphorylated as a result of decreased proximity to the activator. Conversely, as a cell spreads and flattens, the substrate becomes globally phosphorylated because of increased proximity of the substrate to the activator. Similarly, in the leading edge of polarized cells and in protrusions such as lamellipodia or filopodia, the substrate is highly phosphorylated. As a specific test of the model, we found that the experimentally observed preferential activation of the G protein Cdc42 in the periphery of fibroblasts that was recently reported is consistent with model predictions. CONCLUSIONS: We conclude that cell-signaling pathways can theoretically be turned on and off, both locally and globally, in response to alterations in cell size and shape.     

Rate of moult affects feather quality: a mechanism linking current reproductive effort to future survival.

Life-history theory proposes that costs must be associated with reproduction. Many direct costs are incurred during breeding. There is also evidence for indirect costs, incurred after breeding, which decrease survival and future reproductive success. One possible indirect cost identified in birds is that breeding activity in some way compromises plumage quality in the subsequent moult. Here we propose a mechanism by which this could occur. Breeding activity delays the start of moult. Birds that start to moult later also moult more rapidly--an effect of decreasing daylength. Could this result in poorer quality plumage? We kept two groups of male European starlings, Sturnus vulgaris, one on constant long days and the other on decreasing daylengths from the start of moult. Decreasing daylengths reduced the duration of moult from 103 +/- 4 days to 73 +/- 3 days (p < 0.0001). Newly grown primary feathers of birds that moulted fast were slightly shorter, weighed less (p < 0.05) and were more asymmetrical. They had a thinner rachis (p < 0.005), were less hard (p < 0.01) and less rigid (p < 0.05). They were also less resistant to wear so that differences in mass and asymmetry increased with time. There was no difference in Young''s modulus. Poorer quality plumage will lead to decreased survival due to decreased flight performance and increased thermoregulatory costs. Thus, reproduction incurs costs through a mechanism that operates after the end of breeding.