Songs versus colours versus horns: what explains the diversity of sexually selected traits?

Papers on sexual selection often highlight the incredible diversity of sexually selected traits across animals. Yet, few studies have tried to explain why this diversity evolved. Animals use many different types of traits to attract mates and outcompete rivals, including colours, songs, and horns, but it remains unclear why, for example, some taxa have songs, others have colours, and others horns. Here, we first conduct a systematic survey of the basic diversity and distribution of different types of sexually selected signals and weapons across the animal Tree of Life. Based on this survey, we describe seven major patterns in trait diversity and distributions. We then discuss 10 unanswered questions raised by these patterns, and how they might be addressed. One major pattern is that most types of sexually selected signals and weapons are apparently absent from most animal phyla (88%), in contrast to the conventional wisdom that a diversity of sexually selected traits is present across animals. Furthermore, most trait diversity is clustered in Arthropoda and Chordata, but only within certain clades. Within these clades, many different types of traits have evolved, and many types appear to have evolved repeatedly. By contrast, other major arthropod and chordate clades appear to lack all or most trait types, and similar patterns are repeated at smaller phylogenetic scales (e.g. within insects). Although most research on sexual selection focuses on female choice, we find similar numbers of traits (among sampled species) are involved in male contests (44%) and female choice (55%). Overall, these patterns are largely unexplained and unexplored, as are many other fundamental questions about the evolution of these traits. We suggest that understanding the diversity of sexually selected traits may require a shift towards macroevolutionary studies at relatively deep timescales (e.g. tens to hundreds of millions of years ago).     

Structural color change following hydration and dehydration of iridescent mourning dove (Zenaida macroura) feathers

Dynamic changes in integumentary color occur in cases as diverse as the neurologically controlled iridiphores of cephalopod skin and the humidity-responsive cuticles of longhorn beetles. By contrast, feather colors are generally assumed to be relatively static, changing by small amounts only over periods of months. However, this assumption has rarely been tested even though structural colors of feathers are produced by ordered nanostructures that are analogous to those in the aforementioned dynamic systems. Feathers are neither innervated nor vascularized and therefore any color change must be caused by external stimuli. Thus, we here explore how feathers of iridescent mourning doves Zenaida macroura respond to a simple stimulus: addition and evaporation of water. After three rounds of experimental wetting and subsequent evaporation, iridescent feather color changed hue, became more chromatic and increased in overall reflectance by almost 50%. To understand the mechanistic basis of this change, we used electron microscopy to examine macro- and nanostructures before and after treatment. Transmission electron microscopy and transfer matrix thin-film models revealed that color is produced by thin-film interference from a single (∼335 nm) layer of keratin around the edge of feather barbules, beneath which lies a layer of air and melanosomes. After treatment, the most striking morphological difference was a twisting of colored barbules that exposed more of their surface area for reflection, explaining the observed increase in brightness. These results suggest that some plumage colors may be more malleable than previously thought, leading to new avenues for research on dynamic plumage color.     

Does egg carotenoid improve larval quality in Arctic charr (Salvelinus alpinus)?

Females in mutually ornamented species are often less conspicuously ornamented than their male conspecifics. It has been hypothesized that offspring quality may decrease if females invest more resources into ornaments at the expense of resources in eggs. An experiment was carried out to test whether natural variation in carotenoid in the eggs from a wild population of Arctic charr (Salvelinus alpinus) was associated with survival and growth of their offspring until hatching. Wild Arctic charr were caught at a spawning ground during the spawning period. Eggs from two different females, one female with yellowish carotenoid‐rich eggs and one with paler eggs, were fertilized by sperm from the same male. This was repeated until gametes were collected from 42 females and 21 males, giving a total of 21 groups. After fertilization, the zygotes from each of the two females were reared in four replicated groups. These 168 groups were reared separately until hatching when the surviving larvae were counted and their body length measured. For the two response variables survival and body length at hatching, no effect was demonstrated of any of the predictors (i) amount of carotenoid in the unfertilized eggs, (ii) the mothers'' body condition, or (iii) ornament intensity of their red carotenoid‐based abdominal ornament. Thus, this study gives no support for the hypothesis that females investing less carotenoid into their eggs suffer from decreased offspring quality until hatching. This lack of association between female ornament intensity and their fitness is not as expected if female ornaments evolved due to direct sexual selection from males on the more ornamented females (“direct selection hypothesis”).     

Mechanism of the wing colouration in the dragonfly Zenithoptera lanei (Odonata: Libellulidae) and its role in intraspecific communication

Zenithoptera dragonflies are known for their remarkable bluish colouration on their wings and unique male behaviour of folding and unfolding their wings while perching. However, nothing is known about the optical properties of such colouration and its structural and functional background. In this paper, we aimed to study the relationship between the wing membrane ultrastructure, surface microstructure and colour spectra of male wings in Zenithoptera lanei and test the hypothesis that colouration functions as a signal in territorial fights between males. The results show that the specific wing colouration derives from interference in alternating layers of melanized and unmelanized cuticle in the wing membrane, combined with diffuse scattering in two different layers of wax crystals on the dorsal wing surface, one lower layer of long filaments, and one upper layer of leaf-shaped crystals. The results also show that the thicker wax coverage of the dorsal surface of the wings results in increased brightness and reduced chroma. In the field experiments, we have demonstrated that there is a reduction of aggressive reactions of rivals towards individuals with experimentally reduced amount of blue wing colouration.     

Classical autophagy proteins LC3B and ATG4B facilitate melanosome movement on cytoskeletal tracks

Macroautophagy/autophagy is a dynamic and inducible catabolic process that responds to a variety of hormonal and environmental cues. Recent studies highlight the interplay of this central pathway in a variety of pathophysiological diseases. Although defective autophagy is implicated in melanocyte proliferation and pigmentary disorders, the mechanistic relationship between the 2 pathways has not been elucidated. In this study, we show that autophagic proteins LC3B and ATG4B mediate melanosome trafficking on cytoskeletal tracks. While studying melanogenesis, we observed spatial segregation of LC3B-labeled melanosomes with preferential absence at the dendritic ends of melanocytes. This LC3B labeling of melanosomes did not impact the steady-state levels of these organelles but instead facilitated their intracellular positioning. Melanosomes primarily traverse on microtubule and actin cytoskeletal tracks and our studies reveal that LC3B enables the assembly of microtubule translocon complex. At the microtubule-actin crossover junction, ATG4B detaches LC3B from melanosomal membranes by enzymatic delipidation. Further, by live-imaging we show that melanosomes transferred to keratinocytes lack melanocyte-specific LC3B. Our study thus elucidates a new role for autophagy proteins in directing melanosome movement and reveal the unconventional use of these proteins in cellular trafficking pathways. Such crosstalk between the central cellular function and housekeeping pathway may be a crucial mechanism to balance melanocyte bioenergetics and homeostasis.     

Body size does not predict species richness among the metazoan phyla

We present a comparative study of the relationship between body size and described taxonomic diversity in the Metazoa. We find no pattern between body size and taxonomic diversity; neither the smallest organisms nor organisms at an intermediate body size are consistently more diverse than their closest relatives. This conclusion holds for both nonphylogenetic analysis, in which phyla are treated as independent points, and analysis of independent contrasts using several recent hypotheses of metazoan phylogeny. These results appear surprising in the context of existing models of body size distributions. However, such models are built around the prevalence of right‐skewed distributions and we find no evidence for such a distribution.     

Pigmented anatomy in Carboniferous cyclostomes and the evolution of the vertebrate eye

The success of vertebrates is linked to the evolution of a camera-style eye and sophisticated visual system. In the absence of useful data from fossils, scenarios for evolutionary assembly of the vertebrate eye have been based necessarily on evidence from development, molecular genetics and comparative anatomy in living vertebrates. Unfortunately, steps in the transition from a light-sensitive ‘eye spot’ in invertebrate chordates to an image-forming camera-style eye in jawed vertebrates are constrained only by hagfish and lampreys (cyclostomes), which are interpreted to reflect either an intermediate or degenerate condition. Here, we report—based on evidence of size, shape, preservation mode and localized occurrence—the presence of melanosomes (pigment-bearing organelles) in fossil cyclostome eyes. Time of flight secondary ion mass spectrometry analyses reveal secondary ions with a relative intensity characteristic of melanin as revealed through principal components analyses. Our data support the hypotheses that extant hagfish eyes are degenerate, not rudimentary, that cyclostomes are monophyletic, and that the ancestral vertebrate had a functional visual system. We also demonstrate integument pigmentation in fossil lampreys, opening up the exciting possibility of investigating colour patterning in Palaeozoic vertebrates. The examples we report add to the record of melanosome preservation in Carboniferous fossils and attest to surprising durability of melanosomes and biomolecular melanin.     

Evolutionary ecology of specialization: insights from phylogenetic analysis

In this Special feature, we assemble studies that illustrate phylogenetic approaches to studying salient questions regarding the effect of specialization on lineage diversification. The studies use an array of techniques involving a wide-ranging collection of biological systems (plants, butterflies, fish and amphibians are all represented). Their results reveal that macroevolutionary examination of specialization provides insight into the patterns of trade-offs in specialized systems; in particular, the genetic mechanisms of trade-offs appear to extend to very different aspects of life history in different groups. In turn, because a species may be a specialist from one perspective and a generalist in others, these trade-offs influence whether we perceive specialization to have effects on the evolutionary success of a lineage when we examine specialization only along a single axis. Finally, how geographical range influences speciation and extinction of specialist lineages remains a question offering much potential for further insight.     

THE MICRO AND MACRO IN BODY SIZE EVOLUTION

The diversity of body sizes of organisms has traditionally been explained in terms of microevolutionary processes: natural selection owing to differential fitness of individual organisms, or to macroevolutionary processes: species selection owing to the differential proliferation of phylogenetic lineages. Data for terrestrial mammals and birds indicate that even on a logarithmic scale frequency distributions of body mass among species are significantly skewed towards larger sizes. We used simulation models to evaluate the extent to which macro- and microevolutionary processes are sufficient to explain these distributions. Simulations of a purely cladogenetic process with no bias in extinction or speciation rates for different body sizes did not produce skewed log body mass distributions. Simulations that included size-biased extinction rates, especially those that incorporated anagenetic size change within species between speciation and extinction events, regularly produced skewed distributions. We conclude that although cladogenetic processes probably play a significant role in body size evolution, there must also be a significant anagenetic component. The regular variation in the form of mammalian body size distributions among different-sized islands and continents suggests that environmental conditions, operating through both macro- and microevolutionary processes, determine to a large extent the diversification of body sizes within faunas. Macroevolution is not decoupled from microevolution.