DIVERSITY‐DEPENDENT CLADOGENESIS AND TRAIT EVOLUTION IN THE ADAPTIVE RADIATION OF THE AUKS (AVES: ALCIDAE)

Through the course of an adaptive radiation, the evolutionary speed of cladogenesis and ecologically relevant trait evolution are expected to slow as species diversity increases, niches become occupied, and ecological opportunity declines. We develop new likelihood‐based models to test diversity‐dependent evolution in the auks, one of only a few families of seabirds adapted to underwater “flight,” and which exhibit a large variety of bill sizes and shapes. Consistent with the expectations of adaptive radiation, we find both a decline in rates of cladogenesis (a sixfold decline) and bill shape (a 64‐fold decline) evolution as diversity increased. Bill shape diverged into two clades at the basal cladogenesis event with one clade possessing mostly long, narrow bills used to forage primarily on fish, and the other with short thick bills used to forage primarily on plankton. Following this initial divergence in bill shape, size, a known correlate of both prey size and maximum diving depth, diverged rapidly within each of these clades. These results suggest that adaptive radiation in foraging traits underwent initial divergence in bill shape to occupy different food resources, followed by size differentiation to subdivide each niche along the depth axis of the water column.     

Phylogenetic relationships of Neotropical honeycreepers and the evolution of feeding morphology

Phylogenetic relationships among Neotropical honeycreepers were studied by using cytochrome b sequence data. Although honeycreepers were once placed in their own family (Coerebidae), these species did not form a monophyletic group in any of the phylogenies in this study. Thus, our results indicate that nectar-feeding evolved independently multiple times among these birds. The Neotropical honeycreepers are best considered disparate members of a larger radiation of tanagers and finches, in which bill size and shape, and associated feeding behaviors have changed frequently to fill a variety of niches. Our phylogenies also provide specific taxonomic recommendations on the placement of each honeycreeper genus. The use of the taxon Coerebidae is no longer warranted given the well-supported relationships between different honeycreeper species and a variety of tanagers and finches.     

Fitting the bill: do different winter food resources influence juniper titmouse (Baeolophus ridgwayi) bill morphology?

Divergent adaptive selection is a prominent mechanism influencing patterns of morphological diversity. We used the juniper titmouse [Baeolophus ridgwayi (Richmond, 1902)], a nonmigratory passerine that inhabits woodlands throughout western North America, to investigate variation in bill morphology in relation to diet and geography. We gathered data from museum specimens and used morphometric techniques to determine the relative strength of support for competing hypotheses using information theoretics: (1) differences in bill morphology are predicted by a key winter food resource that each regional population consumes (seeds of different juniper tree species); or (2) bill morphology scales with body size, and both increase along a latitudinal gradient. Juniper species emerged as the variable with the most support explaining variation in bill size, supporting the hypothesis that seed sizes influence bill size, independently of body size. The shape analysis revealed no distinct patterns in bill shape variation, but employed a powerful method for evaluating the strength of support for numerous candidate models. The differences in bill size of juniper titmice across their range are likely to reflect adaptive variation, because bill morphology is highly heritable in birds, juniper titmouse gene flow appears to be relatively low, and there is a clear mechanistic explanation for why bill sizes may differ among the ranges of the three juniper species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 667–679.     

Becoming Different But Staying Alike: Patterns of Sexual Size and Shape Dimorphism in Bills of Hummingbirds

Hummingbirds are known for their distinctive patterns of sexual dimorphism, with many species exhibiting sex-related differences in various ecologically-relevant traits, including sex-specific differences in bill shape. It is generally assumed that such patterns are consistent across all hummingbird lineages, yet many taxa remain understudied. In this study we examined patterns of sexual size and sexual shape dimorphism in bills of 32 of 35 species in the monophyletic Mellisugini lineage. We also compared patterns of bill size dimorphism in this group to other hummingbird lineages, using data from 219 hummingbird species. Overall, the presence and degree of sexual size dimorphism was similar across all hummingbird lineages, with the majority of Mellisugini species displaying female-biased sexual size dimorphism, patterns that remain unchanged when analyzed in a phylogenetic context. Surprisingly however, we found that sexual dimorphism in bill shape was nearly absent in the Mellisugini clade, with only 3 of the 32 species examined displaying bill shape dimorphism. Based on observations in other hummingbird lineages, the lack of sexual shape dimorphism in Mellisugini is particularly unusual. We hypothesize that the patterns of sexual size dimorphism observed here may be the consequence of differential selective forces that result from competition for ecological resources. We further propose that an influential mechanism underlying shape dimorphism is competition and niche segregation. Taken together, the evolutionary changes in patterns of sexual shape dimorphism observed in Mellisugini suggest that the evolutionary trends of sexual dimorphism in the Trochilidae are far more dynamic than was previously believed.     

DISCOVERING EXCEPTIONAL DIVERSIFICATIONS AT CONTINENTAL SCALES: THE CASE OF THE ENDEMIC FAMILIES OF NEOTROPICAL SUBOSCINE PASSERINES

The study of continental adaptive radiations has lagged behind research on their island counterparts in part because the mere identification of adaptive radiations is more challenging at continental scales. Here, I demonstrate a new method based on simulations for discovering clades that show exceptionally high phenotypic diversity. The method does not require a phylogeny but accounts for differences in age and species richness among clades and incorporates effects of the phylogenetic structure of data. In addition, I developed a new multivariate measure of phenotypic diversity, which has the advantage over other measures of disparity in that it takes covariation into account. I applied these methods to a clade of endemic Neotropical suboscine passerines, within which the family Furnariidae has been considered an adaptive radiation. I found that the families Thamnophilidae, Furnariidae, and Dendrocolaptidae have experienced a higher rate of cladogenesis than have other clades. Although Thamnophilidae is exceptionally diverse in body size, only Furnariidae and Dendrocolaptidae are exceptionally diverse in shape. The combination of high rates of cladogenesis and high morphometric diversity in traits related to feeding and locomotion suggest that the clade Furnariidae‐Dendrocolaptidae represent an authentic continental adaptive radiation.     

LM and SEM study on the swordfish (Xiphias gladius) tongue

Swordfish (Xiphias gladius L. 1758) is a predatory and migratory fish. Its characteristic feature is a flat and sharp upper jaw forming a “sword”. The adaptation of vertebrates, including fish, to their environment is strictly related to the capacity of feeding and is carried out by often severe modifications of the anatomy of the buccal cavity, especially of the tongue. The aim of this study is, using light and scanning electron microscopy and considering that no data are so far available about the morphology of the tongue in this species, to analyse the anatomical characteristics of the tongue, especially its dorsal surface. The tongue shows a triangular shape and an apex, a body and a root. By SEM the presence of several small denticles and filiform papillae on the latero-ventral body was demonstrated while no taste buds or other sensitive structures are observed. LM shows a squamous stratified epithelium, becoming simple cuboidal around the denticles. Therefore this study could add further data to the knowledges of the fish oral cavity morphology supporting the hypothesis that the modifications and evolution of the tongue anatomy are, also in fish, related to the environment and especially to the feeding habits.     

The adaptive significance of parental role division and sexual size dimorphism in breeding shorebirds

Sexual size dimorphism among 57 species in the shorebird family Scolopacidae is evaluated in relation to parental role division during breeding. Normal size dimorphism, i.e. the female being smaller than the male, occurs in species where the female has the main responsibility for parental care, whereas reverse size dimorphism, the most common pattern among shorebirds, is associated with reversed parental roles. Pronounced dimorphism between sexes occurs, besides in body size, also in bill length, where the sex undertaking the main part of brood attendance has a disproportionately short bill in species adapted for foraging by deep probing. A small body size is of adaptive value to attain high parental efficiency for energetic reasons, because smaller individuals need less energy to maintain themselves. Short bills may be advantageous during brood attendance when feeding mainly takes place in terrestrial habitats together with the chicks. Females released from parental care duties are favoured by a larger body size allowing increased accumulation of energy reserves for egg production. There are obvious parallels between shorebirds and raptors concerning the adaptive significance of reverse sexual size dimorphism and parental role division.     

ADAPTIVE RADIATION AND THE TOPOLOGY OF LARGE PHYLOGENIES

The idea that some organisms possess adaptive features that make them more likely to speciate and/or less likely to go extinct than closely related groups, suggests that large phylogenetic trees should be unbalanced (more species should occur in the group possessing the adaptive features than in the sister group lacking such features). Several methods have been used to document this type of adaptive radiation. One problem with these attempts is that evolutionary biologists may overlook balanced phylogenies while focusing on a few impressively unbalanced ones. To overcome this potential bias, we sampled published large phylogenies without regard to tree shape. These were used to test whether or not such trees are consistently unbalanced. We used recently developed null models to demonstrate that the shapes of large phylogenetic trees: 1) are similar among angiosperms, insects, and tetrapods; 2) differ from those expected due to random selection of a phylogeny from the pool of all trees of similar size; and 3) are significantly more unbalanced than expected if species diverge at random, therefore, conforming to one prediction of adaptive radiation. This represents an important first step in documenting whether adaptive radiation has been a general feature of evolution.     

The evolution of the avian bill as a thermoregulatory organ

The avian bill is a textbook example of how evolution shapes morphology in response to changing environments. Bills of seed‐specialist finches in particular have been the focus of intense study demonstrating how climatic fluctuations acting on food availability drive bill size and shape. The avian bill also plays an important but under‐appreciated role in body temperature regulation, and therefore in energetics. Birds are endothermic and rely on numerous mechanisms for balancing internal heat production with biophysical constraints of the environment. The bill is highly vascularised and heat exchange with the environment can vary substantially, ranging from around 2% to as high as 400% of basal heat production in certain species. This heat exchange may impact how birds respond to heat stress, substitute for evaporative water loss at elevated temperatures or environments of altered water availability, or be an energetic liability at low environmental temperatures. As a result, in numerous taxa, there is evidence for a positive association between bill size and environmental temperatures, both within and among species. Therefore, bill size is both developmentally flexible and evolutionarily adaptive in response to temperature. Understanding the evolution of variation in bill size however, requires explanations of all potential mechanisms. The purpose of this review, therefore, is to promote a greater understanding of the role of temperature on shaping bill size over spatial gradients as well as developmental, seasonal, and evolutionary timescales.     

Variability in seed size selection by granivorous passerines: effects of bird size,bird size variability,and ecological plasticity

The niche variation hypothesis predicts a direct relationship between intraspecific variability in feeding ecology and the variability of the morphological traits related to feeding behaviour. The following study tests this prediction by measuring in captivity the seed size preferences and the morphology of 9–11 individuals of seven specialized granivorous bird species. The average seed size preferences of these birds have previously been shown to be related to components of bill size. The ranges of seed sizes selected were related to the mean bill sizes of birds in a way that paralleled the patterns found when analysing average values. Bill and body size variability were not related, however, to the range of seed preferences after controlling for the significant mean-variance relationship showed by morphological traits. Thus, results do not support the niche variation hypothesis. the significant effect of average bill size on diet variability was consistent with the direct relationship between bird size and ecological plasticity expected on the basis of the shape of the family of functions relating seed size and seed profitability for different-sized birds. These findings suggest morphological mechanisms for ecological plasticity whose generality and evolutionary significance merit further research.     

An introductory ecological biogeography of the Australo-Pacific Meliphagidae

Abstract

The Meliphagidae, that can readily be defined on tongue characteristics, are a monophyletic group centred in the Australo-Pacific region, but with one African genus (Promerops). The classification of Salomonsen (1967) allows 38 genera and 170 species in the former region, and one genus with two species in the latter. Australia and New Guinea jointly have 23 genera and 108 species, and constitute the centre of diversity of the group. Endemic genera are concentrated in Australia and New Guinea, and around the periphery of the Pacific part of the range (Sulawesi, Bonins, Marianas, Hawaii, New Zealand). The meliphagids are diversified in body size and bill form. They are basically nectarivores and insectivores, with most species combining the two roles to varying degrees. There is a good general correlation between bill form and way of life. A few species feed on trunks and aerial flycatching is well developed in many. Morphological modification is only minor in these instances and the meliphagids as a group remain rather generalised in bodily proportions. A long period of coevolution with Australian plant elements is shown by meliphagids being the major pollinators of several tree and shrub genera.

The group combines monotypic genera with restricted ranges and wide-ranging genera with many species. Of the latter; Myzomela, Lichema, and Philemon are centred in the tropics, and Meliphaga and Phylidonyris in Australia. Most of these co-occur over a wide area, this being favoured by differences in body size and bill morphology.

Comparison of three kinds of meliphagid communities, two typical continental ones, two of isolated forest outlyers in Australia, and six insular Pacific ones, shows the first to be rich (10 and 11 genera, 21 and 17 species), and the second impoverished (6 and 7 genera, 9 and 12 species). Individual Pacific island groups, however, have only 2–5 genera, and 3–6 species. Genus to species ratios are 0.55–0.64 in the major continental communities, but are 1.0 in New Zealand and Samoa.

Morphological distance between species, measured as the percent difference in size between successive members along a size gradient is 5.4 and 5.5% for wing length and 4.9 and 9.3% for bill length in the two continental communities. It increases to 7.8–14.9, and 11.3–12.7%, respectively, in the isolated forest outlyers of Tasmania and southwestern Australia. The figures are 23.0 and 35.0% for wing and bill length in New Zealand, and 41.0 and 51.0% in Fijian forms. This accords with current theory that in impoverished insular environments, size separation of co-occurring species must be greater.

The marked success of the Meliphagidae in the Australo-Pacific region can be attributed to their versatility and adaptibility, and dual role of insectivore and nectarivore in an area exceptionally rich in nectar-producing trees and shrubs.     

Beak of the pinch: anti-parasite traits are similar among Darwin’s finch species

Darwin’s finches are an iconic example of adaptive radiation. The size and shape of the beaks of different finch species are diversified for feeding on different size seeds and other food resources. However, beaks also serve other functions, such as preening for the control of ectoparasites. In diverse groups of birds, the effectiveness of preening is governed by the length of the overhanging tip of the upper mandible of the beak. This overhang functions as a template against which the tip of the lower mandible generates a pinching force sufficient to damage or kill ectoparasites. Here we compare feeding versus preening components of the beak morphology of small, medium, and large ground finches that share a single parasite community. Despite adaptive divergence in beak morphology related to feeding, the three species have nearly identical relative mandibular overhang lengths. Moreover, birds with intermediate length overhangs have the lowest feather mite loads. These results suggest that Darwin’s finches maintain an optimal beak morphology to effectively control their ectoparasites.     

Shell size and shape in Madeiran land snails: do niches remain unfilled?

The distribution of shell heights and diameters in the mainly endemic Madeiran land snail fauna shows the bimodal pattern of high- and low-spired shells found in many other faunas. Field and laboratory studies show that shell shape is associated with the angle of substrate on which the snails crawl; as elsewhere, tall spired species use vertical surfaces or burrow in soft material. Flattened species predominate on horizontal surfaces, while globular species are less specific in their preferences. Detailed comparisons with the fauna of N.W. Europe show that the proportion of high-spired species in the Madeiran fauna is low, and large high-spired species associated with vertical surfaces are very few in number despite an apparent abundance of suitable habitats. Amongst low-spired species, one family, the Helicidae, dominates the Madeiran fauna. While the overall distribution of size in these species is much as in Europe, Madeiran helicids extend into smaller size classes than do those in Europe, and they appear to fill a gap in the scatter created by the absence of other families.
Non-endemic species, other than those strictly associated with man-made environments, are generally small in size. In the upper scatter, their size distribution parallels that of endemics, but in the lower scatter they constitute the whole of the smallest size classes.
The role of interspecific competition in determining these distributions is discussed. The range of helicid sizes is compatible with a relaxation of competition or predator pressure relative to other areas, but in the upper scatter there appear to be gaps in the range of size and shape expected despite a long period in which the fauna could evolve. This could indicate the existence of adaptive troughs blocking, or delaying, radiation over the full spectrum of size and shape.     

The role of marker traits in the assortative mating within red crossbills, Loxia curvirostra complex

We conducted mate choice experiments to determine whether differences in calls or bill morphology might influence assortative mating between call types of red crossbills (Loxia curvirostra complex) that have diverged in bill structure to specialize on different species of conifers. Females preferred males that gave calls that matched their own type, but did not prefer males that more closely approximated the average or optimal bill size of the female's call type. These results were consistent with our breeding simulations, which showed that females gained an indirect fitness benefit by choosing a male of her own call type because this reduced the production of offspring with morphologies that fell between adaptive peaks. However, choice based on bill morphology within a call type provided no further benefit. Calls, which crossbills learn from their parents, likely act as a marker trait indicative of the morphological adaptations of the group, allow for easy assessment of potential mates and facilitate rapid divergence under ecological selection.     

Diversity of dermal denticle structure in sharks: Skin surface roughness and three‐dimensional morphology

Shark skin is covered with numerous placoid scales or dermal denticles. While previous research has used scanning electron microscopy and histology to demonstrate that denticles vary both around the body of a shark and among species, no previous study has quantified three‐dimensional (3D) denticle structure and surface roughness to provide a quantitative analysis of skin surface texture. We quantified differences in denticle shape and size on the skin of three individual smooth dogfish sharks (Mustelus canis) using micro‐CT scanning, gel‐based surface profilometry, and histology. On each smooth dogfish, we imaged between 8 and 20 distinct areas on the body and fins, and obtained further comparative skin surface data from leopard, Atlantic sharpnose, shortfin mako, spiny dogfish, gulper, angel, and white sharks. We generated 3D images of individual denticles and measured denticle volume, surface area, and crown angle from the micro‐CT scans. Surface profilometry was used to quantify metrology variables such as roughness, skew, kurtosis, and the height and spacing of surface features. These measurements confirmed that denticles on different body areas of smooth dogfish varied widely in size, shape, and spacing. Denticles near the snout are smooth, paver‐like, and large relative to denticles on the body. Body denticles on smooth dogfish generally have between one and three distinct ridges, a diamond‐like surface shape, and a dorsoventral gradient in spacing and roughness. Ridges were spaced on average 56 µm apart, and had a mean height of 6.5 µm, comparable to denticles from shortfin mako sharks, and with narrower spacing and lower heights than other species measured. We observed considerable variation in denticle structure among regions on the pectoral, dorsal, and caudal fins, including a leading‐to‐trailing edge gradient in roughness for each region. Surface roughness in smooth dogfish varied around the body from 3 to 42 microns.     

Divergence and evolution in Darwin's finches

The medium and large ground finches of the Galapagos archipelago Geospiza fortis and G. magnirostris are distinguished by their different body size and bill dimensions on most of the islands where they both occur. On the island of Indefatigable this distinction is not complete and a group of birds with intermediate bill dimensions is present. The origin of this group could be explained by sympatric divergence of G. fortis or by hybridization, between this species and G. magnirostris . Although the conditions for sympatric divergence are severe it seems likely that strong disruptive selection for different optimal bill sizes may be operating on G. fortis , due to the presence of several ecological niches, separate categories of size and hardness of seeds the birds eat. It is suggested that islands in the Galapagos archipelago, and perhaps other oceanic islands, may provide conditions extremely conducive to sympatric divergence, or even sympatric speciation.     

Evolution of cranial shape in a continental‐scale evolutionary radiation of Australian lizards

A defining character of adaptive radiations is the evolution of a diversity of morphological forms that are associated with the use of different habitats, following the invasion of vacant niches. Island adaptive radiations have been thoroughly investigated but continental scale radiations are more poorly understood. Here, we use 52 species of Australian agamid lizards and their Asian relatives as a model group, and employ three‐dimensional geometric morphometrics to characterize cranial morphology and investigate whether variation in cranial shape reflects patterns expected from the ecological process of adaptive radiation. Phylogenetic affinity, evolutionary allometry, and ecological life habit all play major roles in the evolution of cranial shape in the sampled lizards. We find a significant association between cranial shapes and life habit. Our results are in line with the expectations of an adaptive radiation, and this is the first time detailed geometric morphometric analyses have been used to understand the selective forces that drove an adaptive radiation at a continental scale.     

Phylogenetic relationships and morphological diversity in Darwin's finches and their relatives

Despite the importance of Darwin's finches to the development of evolutionary theory, the origin of the group has only recently been examined using a rigorous, phylogenetic methodology that includes many potential outgroups. Knowing the evolutionary relationships of Darwin's finches to other birds is important for understanding the context from which this adaptive radiation arose. Here we show that analysis of mitochondrial DNA sequence data from the cytochrome b gene confirm that Darwin's finches are monophyletic. In addition, many taxa previously proposed as the sister taxon to Darwin's finches can be excluded as their closest living relative. Darwin's finches are part of a well-supported monophyletic group of species, all of which build a domed nest. All but two of the non-Darwin's finches included in this clade occur on Caribbean islands and most are Caribbean endemics. These close relatives of Darwin's finches show a diversity of bill types and feeding behaviors similar to that observed among Darwin's finches themselves. Recent studies have shown that adaptive evolution in Darwin's finches occurred relatively quickly. Our data show that among the relatives of Darwin's finches, the evolution of bill diversity was also rapid and extensive.     

Structure and variation in the hindlimb musculature of the woodcreepers (Aves: Passeriformes: Dendrocolaptinae)

The Dendrocolaptinae (woodcreepers), a clade of neotropical passerine birds, form an adaptive radiation with a spectrum of body sizes and bill shapes. Woodcreepers are scansorial, climbing vertical tree trunks supported by their forward toes and stiffened tail. The hindlimb musculature was dissected and described for 42 of the 50 species representing all genera, and for 14 outgroup species. Structural, functional, developmental and evolutionary aspects of muscular variations are analysed. Woodcreepers have extensive ossification of leg tendons. There is intraspecific variation in the degree of ossification, and interspecific variation in the occurrence of ossification between muscles. Intraspecific variation in muscle structure was apportioned according to a published classification. Nine muscles showed variation of the minor, singular, mimicking and incongruous types, but explosive variation was lacking. Some muscles are more prone to variation than others. Ten muscles showed interspecific variations of four types, for which new terms are proposed: occurrence variations; attachment variations in origins and insertions; structural variations in size, shape, or fibre arrangement; and relational variations with other muscles. Variations in the presence of a muscle component did not occur. Discrimination of intraspecific variations from interspecific variations is discussed.