Evolution of the ovenbird-woodcreeper assemblage (Aves: Furnariidae) - major shifts in nest architecture and adaptive radiation

The Neotropical ovenbirds (Furnariidae) form an extraordinary morphologically and ecologically diverse passerine radiation, which includes many examples of species that are superficially similar to other passerine birds as a resulting from their adaptations to similar lifestyles. The ovenbirds further exhibits a truly remarkable variation in nest types, arguably approaching that found in the entire passerine clade. Herein we present a genus-level phylogeny of ovenbirds based on both mitochondrial and nuclear DNA including a more complete taxon sampling than in previous molecular studies of the group. The phylogenetic results are in good agreement with earlier molecular studies of ovenbirds, and supports the suggestion that Geositta and Sclerurus form the sister clade to both core-ovenbirds and woodcreepers. Within the core-ovenbirds several relationships that are incongruent with traditional classifications are suggested. Among other things, the philydorine ovenbirds are found to be non-monophyletic. The mapping of principal nesting strategies onto the molecular phylogeny suggests cavity nesting to be plesiomorphic within the ovenbird–woodcreeper radiation. It is also suggested that the shift from cavity nesting to building vegetative nests is likely to have happened at least three times during the evolution of the group. We suggest that the shifts in nest architecture within the furnariine and synallaxine ovenbirds have served as an ecological release that has facilitated diversification into new habitats and new morphological specializations.     

Niche evolution and diversification in a Neotropical radiation of birds (Aves: Furnariidae)

Rapid diversification may be caused by ecological adaptive radiation via niche divergence. In this model, speciation is coupled with niche divergence and lineage diversification is predicted to be correlated with rates of niche evolution. Studies of the role of niche evolution in diversification have generally focused on ecomorphological diversification but climatic‐niche evolution may also be important. We tested these alternatives using a phylogeny of 298 species of ovenbirds (Aves: Furnariidae). We found that within Furnariidae, variation in species richness and diversification rates of subclades were best predicted by rate of climatic‐niche evolution than ecomorphological evolution. Although both are clearly important, univariate regression and multivariate model averaging more consistently supported the climatic‐niche as the best predictor of lineage diversification. Our study adds to the growing body of evidence, suggesting that climatic‐niche divergence may be an important driver of rapid diversification in addition to ecomorphological evolution. However, this pattern may depend on the phylogenetic scale at which rate heterogeneity is examined.     

Molecular data reveal some major adaptational shifts in the early evolution of the most diverse avian family, the Furnariidae

A robust phylogeny estimate for the family Furnariidae (sensu lato) was obtained using sequences of two nuclear introns and one mitochondrial gene (cyt b). Contrary to the widely accepted sister-group relationship of ovenbirds (Furnariinae) and woodcreepers (Dendrocolaptinae), a basal clade is suggested for Sclerurus and Geositta, while Xenops, hitherto considered an aberrant ovenbird, was found to occupy a basal position on the woodcreeper lineage. The morphological variation is re-interpreted in view of this revised phylogenetic hypothesis. Presumably, the remarkable adaptive radiation in this family started as primitive, Sclerurus-likes forms, which used the tail as a prop during terrestrial feeding, lured up to seek food on tree-trunks. The two basal woodcreeper genera, Xenops and then Glyphorynchus, show strong cranial specializations for hammering in wood, thus presenting a remarkable parallelism with the family Picidae, Xenops resembling a piculet, Glyphorynchus, a diminutive woodpecker. However, this specialization was lost in other woodcreepers, which show a more normal passerine skull, adapted for probing and prying in tree-trunk crevices and sallying for escaping insects. The ovenbirds developed a more flexible (rhynchokinetic) bill, well suited for probing and retrieving hidden prey in dead-leaf clusters and debris suspended in the vegetation, and in epiphyte masses. Adaptations to live in open terrain are secondary.Electronic Supplementary Material Supplementary material is available in the online version of this article at http://dx.doi.org/10.1007/s10336-004-0054-5Communicated by A.J. Helbig     

Detecting shifts in diversification rates without fossils

Studies of shifts in diversification rates and adaptive radiations are difficult when there are no fossils because past events cannot be inferred. The phylogenies of recent species, however, allow one to infer the patterns of past diversifications. I present a new method for estimating the diversification rate of a lineage, provided that a phylogeny of recent species, constructed, for instance, with molecular data, is available. This method was inspired by survival models and takes into account species that are not included in detailed phylogenetic data, provided that approximate dates of origin of these species are known. Likelihood ratio tests and Akaike Information Criterion make it possible to test for differences in diversification among lineages or groups of lineages and, thus, to evaluate adaptive radiation hypotheses. The present modeling approach can easily be extended to include temporal variations in diversification rates. A simulation study showed that the method is statistically consistent, avoiding Type I and Type II errors, and that it is robust to periodic or random fluctuations in the speciation rate. An example is presented with a composite phylogeny of primates.     

Lineage diversification and morphological evolution in a large-scale continental radiation: the neotropical ovenbirds and woodcreepers (aves: Furnariidae)

Patterns of diversification in species-rich clades provide insight into the processes that generate biological diversity. We tested different models of lineage and phenotypic diversification in an exceptional continental radiation, the ovenbird family Furnariidae, using the most complete species-level phylogenetic hypothesis produced to date for a major avian clade (97% of 293 species). We found that the Furnariidae exhibit nearly constant rates of lineage accumulation but show evidence of constrained morphological evolution. This pattern of sustained high rates of speciation despite limitations on phenotypic evolution contrasts with the results of most previous studies of evolutionary radiations, which have found a pattern of decelerating diversity-dependent lineage accumulation coupled with decelerating or constrained phenotypic evolution. Our results suggest that lineage accumulation in tropical continental radiations may not be as limited by ecological opportunities as in temperate or island radiations. More studies examining patterns of both lineage and phenotypic diversification are needed to understand the often complex tempo and mode of evolutionary radiations on continents.     

Body mass evolution and diversification within horses (family Equidae)

Horses (family Equidae) are a classic example of adaptive radiation, exhibiting a nearly 60‐fold increase in maximum body mass and a peak taxonomic diversity of nearly 100 species across four continents. Such patterns are commonly attributed to niche competition, in which increased taxonomic diversity drives increased size disparity. However, neutral processes, such as macroevolutionary ‘diffusion’, can produce similar increases in disparity without increased diversity. Using a comprehensive database of Equidae species size estimates and a common mathematical framework, we measure the contributions of diversity‐driven and diffusion‐driven mechanisms for increased disparity during the Equidae radiation. We find that more than 90% of changes in size disparity are attributable to diffusion alone. These results clarify the role of species competition in body size evolution, indicate that morphological disparity and species diversity may be only weakly coupled in general, and demonstrate that large species may evolve from neutral macroevolutionary diffusion processes alone.     

Reconstructing shifts in diversification rates on phylogenetic trees

Few issues in evolutionary biology have received as much attention over the years or have generated as much controversy as those involving evolutionary rates. One unresolved issue is whether or not shifts in speclation and/or extinction rates are closely tied to the origin of 'key' innovations in evolution. This discussion has long been dominated by 'time-based' methods using data from the fossil record. Recently, however, attention has shifted to 'tree-based' methods, in which time, if It plays any role at all, is incorporated secondarily, usually based on molecular data. Tests of hypotheses about key innovations do require Information about phylogenetic relationships, and some of these tests can be implemented without any information about time. However, every effort should be made to obtain information about time, which greatly increases the power of such tests.     

Heterogeneity in the rate of molecular sequence evolution substantially impacts the accuracy of detecting shifts in diversification rates

As species richness varies along the tree of life, there is a great interest in identifying factors that affect the rates by which lineages speciate or go extinct. To this end, theoretical biologists have developed a suite of phylogenetic comparative methods that aim to identify where shifts in diversification rates had occurred along a phylogeny and whether they are associated with some traits. Using these methods, numerous studies have predicted that speciation and extinction rates vary across the tree of life. In this study, we show that asymmetric rates of sequence evolution lead to systematic biases in the inferred phylogeny, which in turn lead to erroneous inferences regarding lineage diversification patterns. The results demonstrate that as the asymmetry in sequence evolution rates increases, so does the tendency to select more complicated models that include the possibility of diversification rate shifts. These results thus suggest that any inference regarding shifts in diversification pattern should be treated with great caution, at least until any biases regarding the molecular substitution rate have been ruled out.     

Likelihood methods for detecting temporal shifts in diversification rates

Maximum likelihood is a potentially powerful approach for investigating the tempo of diversification using molecular phylogenetic data. Likelihood methods distinguish between rate-constant and rate-variable models of diversification by fitting birth-death models to phylogenetic data. Because model selection in this context is a test of the null hypothesis that diversification rates have been constant over time, strategies for selecting best-fit models must minimize Type I error rates while retaining power to detect rate variation when it is present. Here I examine model selection, parameter estimation, and power to reject the null hypothesis using likelihood models based on the birth-death process. The Akaike information criterion (AIC) has often been used to select among diversification models; however, I find that selecting models based on the lowest AIC score leads to a dramatic inflation of the Type I error rate. When appropriately corrected to reduce Type I error rates, the birth-death likelihood approach performs as well or better than the widely used gamma statistic, at least when diversification rates have shifted abruptly over time. Analyses of datasets simulated under a range of rate-variable diversification scenarios indicate that the birth-death likelihood method has much greater power to detect variation in diversification rates when extinction is present. Furthermore, this method appears to be the only approach available that can distinguish between a temporal increase in diversification rates and a rate-constant model with nonzero extinction. I illustrate use of the method by analyzing a published phylogeny for Australian agamid lizards.     

Polyphyly of the hawk genera Leucopternis and Buteogallus (Aves, Accipitridae): multiple habitat shifts during the Neotropical buteonine diversification

Background  

The family Accipitridae (hawks, eagles and Old World vultures) represents a large radiation of predatory birds with an almost global distribution, although most species of this family occur in the Neotropics. Despite great morphological and ecological diversity, the evolutionary relationships in the family have been poorly explored at all taxonomic levels. Using sequences from four mitochondrial genes (12S, ATP8, ATP6, and ND6), we reconstructed the phylogeny of the Neotropical forest hawk genus Leucopternis and most of the allied genera of Neotropical buteonines. Our goals were to infer the evolutionary relationships among species of Leucopternis, estimate their relationships to other buteonine genera, evaluate the phylogenetic significance of the white and black plumage patterns common to most Leucopternis species, and assess general patterns of diversification of the group with respect to species' affiliations with Neotropical regions and habitats.     

Convergent evolution of floral shape tied to pollinator shifts in Iochrominae (Solanaceae)*

Flower form is one of many floral features thought to be shaped by pollinator‐mediated selection. Although the drivers of variation in flower shape have often been examined in microevolutionary studies, relatively few have tested the relationship between shape evolution and shifts in pollination system across clades. In the present study, we use morphometric approaches to quantify shape variation across the Andean clade Iochrominae and estimate the relationship between changes in shape and shifts in pollination system using phylogenetic comparative methods. We infer multiple shifts from an ancestral state of narrow, tubular flowers toward open, bowl‐shaped, or campanulate flowers as well as one reversal to the tubular form. These transitions in flower shape are significantly correlated with changes in pollination system. Specifically, tubular forms tend to be hummingbird‐pollinated and the open forms tend to be insect‐pollinated, a pattern consistent with experimental work as well as classical floral syndromes. Nonetheless, our study provides one of the few empirical demonstrations of the relationship between flower shape and pollination system at a macroevolutionary scale.     

Globin gene family evolution and functional diversification in annelids

Globins are the most common type of oxygen-binding protein in annelids. In this paper, we show that circulating intracellular globin (Alvinella pompejana and Glycera dibranchiata), noncirculating intracellular globin (Arenicola marina myoglobin) and extracellular globin from various annelids share a similar gene structure, with two conserved introns at canonical positions B12.2 and G7.0. Despite sequence divergence between intracellular and extracellular globins, these data strongly suggest that these three globin types are derived from a common ancestral globin-like gene and evolved by duplication events leading to diversification of globin types and derived functions. A phylogenetic analysis shows a distinct evolutionary history of annelid extracellular hemoglobins with respect to intracellular annelid hemoglobins and mollusc and arthropod extracellular hemoglobins. In addition, dehaloperoxidase (DHP) from the annelid, Amphitrite ornata, surprisingly exhibits close phylogenetic relationships to some annelid intracellular globins. We have characterized the gene structure of A. ornata DHP to confirm assumptions about its homology with globins. It appears that it has the same intron position as in globin genes, suggesting a common ancestry with globins. In A. ornata, DHP may be a derived globin with an unusual enzymatic function.     

Temporal shifts in physical habitat of the crayfish,Orconectes neglectus (Faxon)

A total of 300 samples was collected from February 1985 to August 1986 in a medium order Ozark Mountain stream. Physical habitat measurements of temperature, mean water column velocity, depth, and substrate character were recorded for each of the 25 monthly samples along with length and sex of all individuals of Orconectes neglectus (Faxon). Analysis of habitat utilization and suitability (or preference) was conducted using exponential polynomial models of hydraulic stress models. There appeared to be equal preference for depth over the range measured. Both substrate and velocity preference curves were bimodal with each mode designating certain crayfish size classes. Young-of-the-year were found primarily in cobbled, high velocity areas while adults were found in low velocity, macrophyte beds. Utilization curves for laminar sublayer thichness also reflected size-dependent phenomena where young-of-the-year were found in thin sublayer areas and adults were found primarily in thick sublayers. When separated by time and size, adults were found to occupy higher velocity, cobbled habitats during at least two months. This time period corresponded with the time of egg-bearing and further analysis yielded a time-dependent habitat suitability surface which accounted for this movement pattern. We suggest that the application of these suitability surfaces, which reflect habitat changes during the annual life cycle, will produce more accurate predictions of density and will allow better habitat management decisions under various regulated flow scenarios.     

Molecular phylogeographic evidence for multiple shifts in habitat preference in the diversification of an amphipod species

An earlier study of ours demonstrated polygenic control of habitat preference between sympatric populations of an estuarine amphipod (Stanhope et al. 1992). Knowledge of the ecological history in this estuary suggested that two new and distinct habitat types (wood debris and Fucus ) had been formed immediately adjacent to each other, in an area which was previously the habitat type common to the rest of the estuary (bank). This suggested the possibility that the ancestral population had been split into two resource specialists (disruptive selection on habitat preference). The genetic relatedness of these three populations (the proposed ancestor and the two proposed descendants) and six others occupying the same three habitat types were investigated on a regional geographic scale, using an extensive set of genomic DNA RFLPs. These data were combined with measures of habitat preference (including genetic tests) in the additional populations. A very strongly supported phylogeographic tree, unequivocally supported a shift in habitat preference in the wood-debris population of this estuary. The data did not, however, support the hypothesis of disruptive selection on the ancestor (bank) with a consequent split into two resource specialists. Instead, it clearly indicated that the occupants of the Fucus habitat type were members of a habitat specific race, and thus their presence in this estuary reflected the expansion of an old resource base. Furthermore, the combined RFLP and habitat preference data, for all nine populations, indicated that the same polygenically based shift in habitat preference that had occurred in the original estuary had occurred independently, in another estuary, 700 km removed, that had similar environmental circumstances.     

Convergent evolution of morphology and habitat use in the explosive Hawaiian fancy case caterpillar radiation

Species occurring in unconnected, but similar habitats and under similar selection pressures often display strikingly comparable morphology, behaviour and life history. On island archipelagos where colonizations and extinctions are common, it is often difficult to separate whether similar traits are a result of in situ diversification or independent colonization without a phylogeny. Here, we use one of Hawaii's most ecologically diverse and explosive endemic species radiations, the Hawaiian fancy case caterpillar genus Hyposmocoma, to test whether in situ diversification resulted in convergence. Specifically, we examine whether similar species utilizing similar microhabitats independently developed largely congruent larval case phenotypes in lineages that are in comparable, but isolated environments. Larvae of these moths are found on all Hawaiian Islands and are characterized by an extraordinary array of ecomorphs and larval case morphology. We focus on the ‘purse cases’, a group that is largely specialized for living within rotting wood. Purse cases were considered a monophyletic group, because morphological, behavioural and ecological traits appeared to be shared among all members. We constructed a phylogeny based on nuclear and mitochondrial DNA sequences from 38 Hyposmocoma species, including all 14 purse case species and 24 of non‐purse case congeners. Divergence time estimation suggests that purse case lineages evolved independently within dead wood and developed nearly identical case morphology twice: once on the distant Northwest Hawaiian Islands between 15.5 and 9 Ma and once on the younger main Hawaiian Islands around 3.0 Ma. Multiple ecomorphs are usually found on each island, and the ancestral ecomorph of Hyposmocoma appears to have lived on tree bark. Unlike most endemic Hawaiian radiations that follow a clear stepwise progression of colonization, purse case Hyposmocoma do not follow a pattern of colonization from older to younger island. We postulate that the diversity of microhabitats and selection from parasitism/predation from endemic predators may have shaped case architecture in this extraordinary endemic radiation of Hawaiian insects.     

Origin, diversification, and evolution of Samolus valerandi (Samolaceae, Ericales)

The almost cosmopolitan distribution of Samolus valerandi is unique in the genus Samolus L. (Samolaceae), which also includes 12–15 taxa with distributions restricted to smaller areas of the Southern Hemisphere. Recent molecular phylogenetic studies based on chloroplast and nuclear DNA sequences showed that the widespread S. valerandi and the North American S. parviflorus are both part of a strongly supported clade, together with the North American S. vagans, S. spathulatus, and S. latifolius. To better understand the origin, distribution, and diversification of S. valerandi and to clarify the relationships within this clade, we performed molecular phylogenetic analyses based on the plastid trnS-G intergenic spacer and the nuclear ribosomal ITS region. We have also sought further support for relationships by examining flower and leaf characters. On the basis of new results, we propose that S. valerandi, S. parviflorus, and S. vagans are considered as part of a widespread “species complex”, with its centre of diversity in North America. No clear vicariance patterns were found regarding the phylogeography of S. valerandi, which thus seems to have dispersed secondarily to various places around the world, possibly as a result of human activities.     

Convergent evolution of phenotypic integration and its alignment with morphological diversification in Caribbean Anolis ecomorphs

The adaptive landscape and the G-matrix are keys concepts for understanding how quantitative characters evolve during adaptive radiation. In particular, whether the adaptive landscape can drive convergence of phenotypic integration (i.e., the pattern of phenotypic variation and covariation summarized in the P-matrix) is not well studied. We estimated and compared P for 19 morphological traits in eight species of Caribbean Anolis lizards, finding that similarity in P among species was not correlated with phylogenetic distance. However, greater similarity in P among ecologically similar Anolis species (i.e., the trunk-ground ecomorph) suggests the role of convergent natural selection. Despite this convergence and relatively deep phylogenetic divergence, a large portion of eigenstructure of P is retained among our eight focal species. We also analyzed P as an approximation of G to test for correspondence with the pattern of phenotypic divergence in 21 Caribbean Anolis species. These patterns of covariation were coincident, suggesting that either genetic constraint has influenced the pattern of among-species divergence or, alternatively, that the adaptive landscape has influenced both G and the pattern of phenotypic divergence among species. We provide evidence for convergent evolution of phenotypic integration for one class of Anolis ecomorph, revealing yet another important dimension of evolutionary convergence in this group.