Evolution, biogeography, and patterns of diversification in passerine birds

This paper summarizes and discusses the many new insights into passerine evolution gained from an increased general interest in avian evolution among biologists, and particularly from the extensive use of DNA sequence data in phylogenetic reconstruction. The sister group relationship between the New Zealand rifleman and all other passerines, indicates the importance of the former southern supercontinent Gondwana in the earliest evolution of this group. Following the break-up of Gondwana, the ancestors of other major passerine groups became isolated in Australia (oscines), South America (New World suboscines), and possibly, the then connected Kerguelen Plateau/India/Madagascar tectonic plates (Old World suboscines). The oscines underwent a significant radiation in the Australo-Papuan region and only a few oscine lineages have spread further than to the nearby Southeast Asia. A remarkable exception is the ancestor to the vast Passerida radiation, which now comprises 35% of all bird species. This group obviously benefitted greatly from the increased diversity in plant seed size and morphology during the Tertiary. The lyrebirds (and possibly scrub-birds) constitute the sister group to all other oscines, which renders "Corvida" ( sensu Sibley and Ahlquist 1990) paraphyletic. Sequence data suggests that Passerida, the other clade of oscines postulated based on the results of DNA–DNA hybridizations, is monophyletic, and that the rockfowl and rock-jumpers are the most basal members of this clade. The suboscines in the Old World (Eurylamides) and the New World (Tyrannides), respectively, are sister groups. A provisional, working classification of the passerines is presented based on the increased understanding of the major patterns of passerine evolution.     

Energetics in Liolaemini lizards: implications of a small body size and ecological conservatism

Liolaemini lizards occur in southern South America in a variety of dietary habits across a broad latitudinal and altitudinal distribution. We studied standard metabolic rates of 19 Liolaemini species and analyzed these data using both conventional and phylogenetically informed statistics. Oxygen consumption showed a significant and positive relationship with body mass (SMR = 0.109 × body mass^0.876±0.023), with a higher slope than that expected on the basis of the three-quarter power law model. After phylogenetically informed and conventional analyses, no significant differences in metabolic rates were found to be related to diet or elevation. We hypothesize that small body size, ecological conservatism and physiological compensation may explain the lack of differences in metabolic rates observed among these lizards.     

The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions

Summit metabolic rate ( M_sum , maximum cold-induced metabolic rate) is positively correlated with cold tolerance in birds, suggesting that high M_sum is important for residency in cold climates. However, the phylogenetic distribution of high M_sum among birds and the impact of its evolution on current distributions are not well understood. Two potential adaptive hypotheses might explain the phylogenetic distribution of high M_sum among birds. The cold adaptation hypothesis contends that species wintering in cold climates should have higher M_sum than species wintering in warmer climates. The flight adaptation hypothesis suggests that volant birds might be capable of generating high M_sum as a byproduct of their muscular capacity for flight; thus, variation in M_sum should be associated with capacity for sustained flight, one indicator of which is migration. We collected M_sum data from the literature for 44 bird species and conducted both conventional and phylogenetically informed statistical analyses to examine the predictors of M_sum variation. Significant phylogenetic signal was present for log body mass, log mass-adjusted M_sum , and average temperature in the winter range. In multiple regression models, log body mass, winter temperature, and clade were significant predictors of log M_sum . These results are consistent with a role for climate in determining M_sum in birds, but also indicate that phylogenetic signal remains even after accounting for associations indicative of adaptation to winter temperature. Migratory strategy was never a significant predictor of log M_sum in multiple regressions, a result that is not consistent with the flight adaptation hypothesis.     

The learning advantage: bird species that learn their song show a tighter adjustment of song to noisy environments than those that do not learn

Song learning has evolved within several avian groups. Although its evolutionary advantage is not clear, it has been proposed that song learning may be advantageous in allowing birds to adapt their songs to the local acoustic environment. To test this hypothesis, we analysed patterns of song adjustment to noisy environments and explored their possible link to song learning. Bird vocalizations can be masked by low‐frequency noise, and birds respond to this by singing higher‐pitched songs. Most reports of this strategy involve oscines, a group of birds with learning‐based song variability, and it is doubtful whether species that lack song learning (e.g. suboscines) can adjust their songs to noisy environments. We address this question by comparing the degree of song adjustment to noise in a large sample of oscines (17 populations, 14 species) and suboscines (11 populations, 7 species), recorded in Brazil (Manaus, Brasilia and Curitiba) and Mexico City. We found a significantly stronger association between minimum song frequency and noise levels (effect size) in oscines than in suboscines, suggesting a tighter match in oscines between song transmission capacity and ambient acoustics. Suboscines may be more vulnerable to acoustic pollution than oscines and thus less capable of colonizing cities or acoustically novel habitats. Additionally, we found that species whose song frequency was more divergent between populations showed tighter noise–song frequency associations. Our results suggest that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution of song learning and plasticity.     

COMPARATIVE ANALYSIS OF ACOUSTIC STRUCTURE OF PASSERINE AND WOODPECKER NESTLING CALLS

ABSTRACT

We examined the acoustic structure of the calls of 71 species of nestling passerines (both suboscines and oscines) and 4 species of nestling woodpeckers. Calls varied greatly in general acoustic structure, frequency (pitch) and duration. Some phylogenetic trends occurred, e.g. calls of woodpeckers and suboscines tended to be simpler than those of most oscines. Body size was significantly correlated with both maximum and minimum frequency. Age-related changes occurred in some species but not others. The results suggest some phylogenetic and developmental constraints on call structure, but do not rule out the possibility that selection acts directly on nestling calls. However, the hypothesis that cavity-nesters would have more easily localizable calls than open-nesters because of lowered predation risk was not supported by our study, which showed no significant differences in any frequency or temporal measures of acoustic structure between cavity-nesters and open-nesters.     

Different frequency control mechanisms and the exploitation of frequency space in passerines

1. Birdsong is used in reproductive context and, consequently, has been shaped by strong natural and sexual selection. The acoustic performance includes a multitude of acoustic and temporal characteristics that are thought to honestly reveal the quality of the singing individual.
2. One major song feature is frequency and its modulation. Sound frequency can be actively controlled, but the control mechanisms differ between different groups. Two described mechanisms are pressure‐driven frequency changes in suboscines and control by syringeal muscles in oscines.
3. To test to what degree these different control mechanisms enhance or limit the exploitation of frequency space by individual species and families, we compared the use of frequency space by tyrannid suboscines and emberizid/passerellid oscines.
4. We find that despite the different control mechanisms, the songs of species in both groups can contain broad frequency ranges and rapid and sustained frequency modulation (FM). The maximal values for these parameters are slightly higher in oscines.
5. Furthermore, the mean frequency range of song syllables is substantially larger in oscines than suboscines. Species within each family group collectively exploit equally broadly the available frequency space.
6. The narrower individual frequency ranges of suboscines likely indicate morphological specialization for particular frequencies, whereas muscular control of frequency facilitated broader exploitation of frequency space by individual oscine species.

     

A latitudinal gradient in rates of evolution of avian syllable diversity and song length

We ask whether rates of evolution in traits important for reproductive isolation vary across a latitudinal gradient, by quantifying evolutionary rates of two traits important for pre-mating isolation-avian syllable diversity and song length. We analyse over 2500 songs from 116 pairs of closely related New World passerine bird taxa to show that evolutionary rates for the two main groups of passerines-oscines and suboscines-doubled with latitude in both groups for song length. For syllable diversity, oscines (who transmit song culturally) evolved more than 20 times faster at high latitudes than in low latitudes, whereas suboscines (whose songs are innate in most species and who possess very simple song with few syllable types) show no clear latitudinal gradient in rate. Evolutionary rates in oscines and suboscines were similar at tropical latitudes for syllable complexity as well as for song length. These results suggest that evolutionary rates in traits important to reproductive isolation and speciation are influenced by latitude and have been fastest, not in the tropics where species diversity is highest, but towards the poles.     

Basal rate of metabolism and temperature regulation of two desert herbivorous octodontid rodents: Octomys mimax and Tympanoctomys barrerae

Summary We studied the energetics of two herbivorous desert rodents from South America. The two species had slightly lower basal metabolic rates, lower thermal conductances, and higher temperature differentials than those expected from their body mass. Mass-independent basal rates of metabolism were higher than those reported for seed-eating desert rodents from North America. Our observations support the hypothesis that desert rodents that eat foods with high water content have higher mass-independent metabolic rates than seed-eating desert rodents.     

Evolution and plasticity: Divergence of song discrimination is faster in birds with innate song than in song learners in Neotropical passerine birds

Plasticity is often thought to accelerate trait evolution and speciation. For example, plasticity in birdsong may partially explain why clades of song learners are more diverse than related clades with innate song. This “song learning” hypothesis predicts that (1) differences in song traits evolve faster in song learners, and (2) behavioral discrimination against allopatric song (a proxy for premating reproductive isolation) evolves faster in song learners. We tested these predictions by analyzing acoustic traits and conducting playback experiments in allopatric Central American sister pairs of song learning oscines (N = 42) and nonlearning suboscines (N = 27). We found that nonlearners evolved mean acoustic differences slightly faster than did leaners, and that the mean evolutionary rate of song discrimination was 4.3 times faster in nonlearners than in learners. These unexpected results may be a consequence of significantly greater variability in song traits in song learners (by 54–79%) that requires song‐learning oscines to evolve greater absolute differences in song before achieving the same level of behavioral song discrimination as nonlearning suboscines. This points to “a downside of learning” for the evolution of species discrimination, and represents an important example of plasticity reducing the rate of evolution and diversification by increasing variability.     

Intraspecific correlations of basal and maximal metabolic rates in birds and the aerobic capacity model for the evolution of endothermy

The underlying assumption of the aerobic capacity model for the evolution of endothermy is that basal (BMR) and maximal aerobic metabolic rates are phenotypically linked. However, because BMR is largely a function of central organs whereas maximal metabolic output is largely a function of skeletal muscles, the mechanistic underpinnings for their linkage are not obvious. Interspecific studies in birds generally support a phenotypic correlation between BMR and maximal metabolic output. If the aerobic capacity model is valid, these phenotypic correlations should also extend to intraspecific comparisons. We measured BMR, M(sum) (maximum thermoregulatory metabolic rate) and MMR (maximum exercise metabolic rate in a hop-flutter chamber) in winter for dark-eyed juncos (Junco hyemalis), American goldfinches (Carduelis tristis; M(sum) and MMR only), and black-capped chickadees (Poecile atricapillus; BMR and M(sum) only) and examined correlations among these variables. We also measured BMR and M(sum) in individual house sparrows (Passer domesticus) in both summer, winter and spring. For both raw metabolic rates and residuals from allometric regressions, BMR was not significantly correlated with either M(sum) or MMR in juncos. Moreover, no significant correlation between M(sum) and MMR or their mass-independent residuals occurred for juncos or goldfinches. Raw BMR and M(sum) were significantly positively correlated for black-capped chickadees and house sparrows, but mass-independent residuals of BMR and M(sum) were not. These data suggest that central organ and exercise organ metabolic levels are not inextricably linked and that muscular capacities for exercise and shivering do not necessarily vary in tandem in individual birds. Why intraspecific and interspecific avian studies show differing results and the significance of these differences to the aerobic capacity model are unknown, and resolution of these questions will require additional studies of potential mechanistic links between minimal and maximal metabolic output.     

Specific chicken repeat 1 (CR1) retrotransposon insertion suggests phylogenetic affinity of rockfowls (genus Picathartes) to crows and ravens (Corvidae)

While the monophyly of the order Passeriformes as well as its suborders suboscines (Tyranni) and oscines (Passeri) is well established, both on morphological and molecular grounds, lower phylogenetic relationships have been a continuous matter of debate, especially within oscines. This is particularly true for the rockfowls (genus Picathartes), which phylogenetic classification has been an ongoing puzzle. Sequence-based molecular studies failed in deriving unambiguously resolved and supported hypotheses. We present here a novel approach: use of retrotransposon insertions as phylogenetic markers in passerine birds. Chicken repeat 1 (CR1) is the most important non-LTR retrotransposon in birds. We present two truncated CR1 loci in passerine birds, not only found in representatives of Corvinae (jays, crows and allies), but also in the West-African Picathartes species which provide new evidence for a closer relationship of these species to Corvidae than has previously been thought. Additionally, we show that not only the absence/presence pattern of a CR1 insertion, but also the CR1 sequences themselves contain phylogenetic information.     

Neighbor-stranger discrimination by song in a suboscine bird, the alder flycatcher, Empidonax alnorum

Bird song and its functions have been studied extensively formore than 50 years, but almost entirely in oscine passerines.Few studies have investigated any aspect of song in suboscinepasserines. This is significant because song development andthe extent of individual variation in song differs greatly betweenthese groups. Learning and auditory feedback play major rolesin song development in all oscines studied, but apparently nopart in song ontogeny in suboscines. The ability of territorialoscine males to discriminate between songs of neighbors andstrangers has received considerable attention, but this phenomenonis virtually unstudied in suboscines. We tested whether a suboscinebird, the alder flycatcher (Empidonax alnorum), was able todiscriminate between songs of neighbors and strangers despitelimited individual variation in song. We performed playbackexperiments to measure responses of males to songs of neighborsand strangers broadcast from the territory boundary shared bythe subject and the neighbor. Subjects responded more aggressivelyto songs of strangers than to songs of neighbors. These resultsfurther our understanding of the evolution of song and its functionsin suboscines by demonstrating that, similar to their oscinerelatives, they can discriminate between the songs of neighborsand strangers.     

Seasonal metabolic acclimatization in mountain chickadees and juniper titmice

Mountain chickadees and juniper titmice from northern Utah were examined to determine metabolic and body-composition characteristics associated with seasonal acclimatization. These species use behavioral adaptations and nocturnal hypothermia, which reduce energetic costs. These adjustments could reduce the need for extensive metabolic adjustments typically found in small passerines that overwinter in cold regions. In addition, these species live at higher altitudes, which may also decrease metabolic acclimatization found in birds. Winter birds tolerated colder test temperatures than summer birds. This improved cold tolerance was associated with an increase in maximal thermogenic capacity or summit metabolism (M(sum)). Winter M(sum) exceeded summer M(sum) by 26.1% in chickadees and 16.2% in titmice. Basal metabolic rates (BMR) were also significantly higher in winter birds compared with summer birds. Pectoralis wet muscle mass increased 33.3% in chickadees and 24.1% in titmice in winter and paralleled the increased M(sum) and BMR. Dry mass of contour plumage increased in winter for both species and was associated with decreased thermal conductance in winter chickadees compared to summer chickadees. Chickadees and titmice show metabolic acclimatization similar to other temperate species.     

Characterization and assessment of an avian repetitive DNA sequence as an icterid phylogenetic marker.

The first tandemly repeated sequence examined in a passerine bird, a 431-bp PstI fragment named pMAT1, has been cloned from the genome of the brown-headed cowbird (Molothrus ater). The sequence represents about 5-10% of the genome (about 4 x 10(5) copies) and yields prominent ethidium bromide stained bands when genomic DNA cut with a variety of restriction enzymes is electrophoresed in agarose gels. A particularly striking ladder of fragments is apparent when the DNA is cut with HinfI, indicative of a tandem arrangement of the monomer. The cloned PstI monomer has been sequenced, revealing no internal repeated structure. There are sequences that hybridize with pMAT1 found in related nine-primaried oscines but not in more distantly related oscines, suboscines, or nonpasserine species. Little sequence similarity to tandemly repeated PstI cut sequences from the merlin (Falco columbarius), saurus crane (Grus antigone), or Puerto Rican parrot (Amazona vittata) or to HinfI digested sequence from the Toulouse goose (Anser anser) was detected. The isolated sequence was used as a probe to examine DNA samples of eight members of the tribe Icterini. This examination revealed phylogenetically informative characters. The repeat contains cutting sites from a number of restriction enzymes, which, if sufficiently polymorphic, would provide new phylogenetic characters. Sequences like these, conserved within a species, but variable between closely related species, may be very useful for phylogenetic studies of closely related taxa.     

Thermogenic capabilities of the opossum Monodelphis domestica when warm and cold acclimated: similarities between American and Australian marsupials

1. Monodelphis domestica is a small marsupial mammal from South America. Its thermogenic abilities in the cold were determined when the opossums were both warm (WA) and cold (CA) acclimated. Maximum heat production of M. domestica was obtained at low temperatures in helium-oxygen. 2. Basal metabolic rate (BMR) in the WA animals was 3.2 W/kg and mean body temperature was 32.6 degrees C at 30 degrees C. These values were lower than those generally reported for marsupials. Nevertheless, these M. domestica showed considerable metabolic expansibility in response to cold. Sustained (summit) metabolism was 8-9 times BMR, while peak metabolism was 11-13 times BMR. These maximum values were equal to, or above, those expected in small placentals. 3. Cold acclimation altered the thermal responses of M. domestica, particularly in warm TaS. However, summit metabolism was not significantly increased; nor did M. domestica show a significant thermogenic response to noradrenaline, which in many small placentals elicits non-shivering thermogenesis. The thermoregulatory responses of this American marsupial were, in most aspects, similar to those of Australian marsupials. This suggests that the considerable thermoregulatory abilities of marsupials are of some antiquity.     

Scaling of swim speed in breath-hold divers

1. Breath-hold divers are widely assumed to descend and ascend at the speed that minimizes energy expenditure per distance travelled (the cost of transport (COT)) to maximize foraging duration at depth. However, measuring COT with captive animals is difficult, and empirical support for this hypothesis is sparse. 2. We examined the scaling relationship of swim speed in free-ranging diving birds, mammals and turtles (37 species; mass range, 0·5-90,000 kg) with phylogenetically informed statistical methods and derived the theoretical prediction for the allometric exponent under the COT hypothesis by constructing a biomechanical model. 3. Swim speed significantly increased with mass, despite considerable variations around the scaling line. The allometric exponent (0·09) was statistically consistent with the theoretical prediction (0·05) of the COT hypothesis. 4. Our finding suggests a previously unrecognized advantage of size in divers: larger animals swim faster and thus could travel longer distance, search larger volume of water for prey and exploit a greater range of depths during a given dive duration. 5. Furthermore, as predicted from the model, endotherms (birds and mammals) swam faster than ectotherms (turtles) for their size, suggesting that metabolic power production limits swim speed. Among endotherms, birds swam faster than mammals, which cannot be explained by the model. Reynolds numbers of small birds (<2 kg) were close to the lower limit of turbulent flow (～ 3 × 10(5) ), and they swam fast possibly to avoid the increased drag associated with flow transition.     

On the rarity of big fierce carnivores and primacy of isolation and area: tracking large mammalian carnivore diversity on two isolated continents

The hypothesis that low productivity has uniquely constrained Australia's large mammalian carnivore diversity, and by inference the biota in general, has become an influential backdrop to interpretations of ecology on the island continent. Whether low productivity has been primary impacts broadly on our understanding of mammalian biogeography, but investigation is complicated by two uniquely Australian features: isolation and the dominance of marsupials. However, until the great American biotic interchange (GABI), South America was also isolated and dominated by pouched carnivores. Here, we examine the low-productivity hypothesis empirically, by comparing large mammalian carnivore diversities in Australia and South America over the past 25 Myr. We find that pre-GABI diversity in Australia was generally comparable to or higher than diversity in South America. Post-GABI, South American diversity rose dramatically, pointing to isolation and phylogenetic constraint as primary influences. Landmass area is another important factor. Comparisons of diversity among the world's seven largest inhabited landmasses show that large mammalian hypercarnivore diversity in Australia approached levels predicted on the basis of landmass area in Late Pleistocene-Recent times, but large omnivore diversity was low. Large marsupial omnivores also appear to have been rare in South America. Isolation and competition with large terrestrial birds and cryptic omnivore taxa may have been more significant constraints in this respect. Relatively high diversity has been achieved in Late Quaternary America, possibly as a result of 'artificially' high immigration or origination rates, whereas that in contemporaneous Africa has been surprisingly poor. We conclude that isolation and landmass area, rather than productivity, are the primary constraints on large mammalian carnivore diversity. Our results quantify the rarity of large hypercarnivorous mammals worldwide.     

Continental drift, paleoclimatology, and the evolution and biogeography of birds

An analysis is presented of the influence that late Mesozoic and Tertiary paleogeography and paleoclimatology may have had on the evolution and biogeography of birds. Many intercontinental connections, especially in the Southern Hemisphere, persisted until the late Cretaceous and/or early Tertiary. Moreover, climates at these times were warmer and more equable than in the late Tertiary, and birds could breed in and disperse through high latitudes. It is concluded that a number of avian orders and families had their origin in Gondwanaland and predrift configurations of the continents were major determinants of their biogeography. Penguins, ratites, galliforms, and suboscines among others are the best examples. Tropical-subtropical Eurasia was probably the centre of origin for the oscines, and primitive stocks entered the New World mostly through Beringia and mostly prior to the Miocene (but also via a North Atlantic land connection prior to the early Eocene). Continental drift and paleoclimatology have clearly influenced the evolution and biogeography of birds, and future advances in the systematics of the higher taxa will undoubtedly provide further confirmation of this.     

Molecular phylogenetics and diversification of the genus Sporophila (Aves: Passeriformes)

The evolutionary affinities within and among many groups of nine-primaried oscines remain unresolved. One such group is Sporophila, a large genus of New World tanager-finches. Our study focused particularly on clarifying the relationship between this genus and a closely related one, Oryzoborus, and on examining the phylogenetic affinities of the "capuchinos," a group of 11 Sporophila species that share a similar male plumage coloration pattern. Our phylogenetic analyses, based on 498 bp of mitochondrial DNA sequence, indicated that: (1) Oryzoborus is embedded within a well-supported clade containing all Sporophila species, which strongly suggests that both genera should be merged, (2) the species of capuchinos comprise a monophyletic group, implying that the plumage patterns common to all probably arose only once, and (3) the capuchinos clade is comprised of two sub-clades, one including two species that are distributed in northern South America and the other one containing eight species that are present south of the Amazon River. Mean sequence divergence among the southern capuchinos species was extremely low, suggesting a rapid radiation within the last half-million years that may be related to the high level of sexual selection present in the genus and might have been promoted by marine ingressions and egressions that occurred in some southern coastal regions of South America in the Late Pleistocene.     

Phylogenetic relationships and historical biogeography of neotropical parrots (Psittaciformes: Psittacidae: Arini) inferred from mitochondrial and nuclear DNA sequences

Previous hypotheses of phylogenetic relationships among Neotropical parrots were based on limited taxon sampling and lacked support for most internal nodes. In this study we increased the number of taxa (29 species belonging to 25 of the 30 genera) and gene sequences (6388 base pairs of RAG-1, cyt b, NADH2, ATPase 6, ATPase 8, COIII, 12S rDNA, and 16S rDNA) to obtain a stronger molecular phylogenetic hypothesis for this group of birds. Analyses of the combined gene sequences using maximum likelihood and Bayesian methods resulted in a well-supported phylogeny and indicated that amazons and allies are a sister clade to macaws, conures, and relatives, and these two clades are in turn a sister group to parrotlets. Key morphological and behavioral characters used in previous classifications were mapped on the molecular tree and were phylogenetically uninformative. We estimated divergence times of taxa using the molecular tree and Bayesian and penalized likelihood methods that allow for rate variation in DNA substitutions among sites and taxa. Our estimates suggest that the Neotropical parrots shared a common ancestor with Australian parrots 59 Mya (million of years ago; 95% credibility interval (CrI) 66, 51 Mya), well before Australia separated from Antarctica and South America, implying that ancestral parrots were widespread in Gondwanaland. Thus, the divergence of Australian and Neotropical parrots could be attributed to vicariance. The three major clades of Neotropical parrots originated about 50 Mya (95% CrI 57, 41 Mya), coinciding with periods of higher sea level when both Antarctica and South America were fragmented with transcontinental seaways, and likely isolated the ancestors of modern Neotropical parrots in different regions in these continents. The correspondence between major paleoenvironmental changes in South America and the diversification of genera in the clade of amazons and allies between 46 and 16 Mya suggests they diversified exclusively in South America. Conversely, ancestors of parrotlets and of macaws, conures, and allies may have been isolated in Antarctica and/or the southern cone of South America, and only dispersed out of these southern regions when climate cooled and Antarctica became ice-encrusted about 35 Mya. The subsequent radiation of macaws and their allies in South America beginning about 28 Mya (95% CrI 22, 35 Mya) coincides with the uplift of the Andes and the subsequent formation of dry, open grassland habitats that would have facilitated ecological speciation via niche expansion from forested habitats.