Joint effects of feeding and breeding behaviour on trophic dimorphism in hummingbirds

A survey of 166 hummingbird species reveals novel associations of bill-length sexual dimorphism (BLSD) with plumage and breeding behaviours. Across all species, female bills become proportionately longer than male bills (higher female-to-male BLSD ratio) as sexual dichromatism increases. However, male bills are proportionately longer (lower female-to-male BLSD ratio) in both lekkers (traditional group display) and clustered breeders (female harems or colonial nests) compared with dispersed breeders. The overall positive association of plumage with BLSD suggests that social status determines priority of access to nectar-providing flowers. Furthermore, the distinctive BLSD associated with breeding aggregations may arise from behaviours that impose constraints on the usual male priority at flowers: female dominance over males around nest colonies and male residence on lek-mating territories. These various factors appear to alter plumage and bill characters of both sexes to produce the range of dimorphisms within the various dispersed and aggregated breeding system categories. Feedback loops caused by ecological consequences of breeding behaviour may alter the evolutionary dynamics of breeding systems, bird-plant interactions, and competing pollinators, as well as help explain the lek paradox.     

Patagial complex evolution in hummingbirds and swifts (Apodiformes): a molecular phylogenetic perspective

Studies of the role of flight in vertebrate evolution often have focused on the propatagial muscle complex because this structure forms the wing's leading edge. However, historical narratives about the evolution of flight anatomy are compromised because traditional higher-level taxonomies typically are based in part on the propatagium itself. To avoid this circularity, I used a consensus molecular phylogeny to examine propatagial evolution in the highly aerial sister groups, hummingbirds and swifts (Apodiformes). Mapping of anatomy on molecular-based phylogeny indicates that structural variation in M .  tensor propatagialis pars brevis (TPB) is congruent with the major subclades of both hummingbirds and swifts. However, the humeral tendon and broad attachment of the fleshy belly of TPB with M .  extensor metacarpi radialis (EMR) most likely underwent parallel change in hummingbirds and swifts, while the distal tendon present only in hummingbirds changed from a thin sheet to a strong tendon. The combination of divergent (within hummingbirds or swifts) and parallel (between hummingbirds and swifts) evolutionary patterns implies that the taxonomic value of the propatagial complex in apodiformes depends on anatomical component and level of divergence. The congruence of anatomy with molecular phylogeny provides independent criteria for designating relatively ancestral versus derived clades of apodiformes. Based on these polarities, living hummingbirds and swifts express additional parallel trends from arboreal to more aerial foraging styles, and from depauperate to species-rich clades. Within apodiformes, the link of flight anatomy with taxonomic and ecologic diversity suggests that elaboration of locomotor modes was important for apodiform diversification, echoing a similar pattern for birds relative to their reptilian ancestors.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 211–219.     

Experimental analysis of variance for DNA hybridization: II. Precision

Using DNAs from the Virginia opossum (Didelphis virginiana), we estimated the variance components for two classes of replicate hybrids: different drivers matched to the same tracer and different homoduplexes made from tracers matched to identical drivers. A nested analysis of variance (ANOVA) was used to partition total variance among four levels: Individuals, extracts, preparations, and different aliquots from the same preparation. The variance contributed by these levels depended on the kind of hybrid replicate (driver or tracer) and on the index of thermal stability (T_mode, T_m, T₅₀H, or Normalized Percentage Hybridization). For replicate drivers, significant variance contributions were made by (1) individuals to T_m, (2) extracts to T_mode and NPH but not T_m, and (3) different preparations to NPH. The composite T₅₀H measure calculated from both T_m and NPH revealed effects from both constituent indices. For replicate tracers, preparation error was the single most consistent effect across all indices, followed by extract effects for those indices that incorporated a measure of percent hybridization (T₅₀H NPH). Total variance of the four indices was qualitatively similar for both drivers and tracers: T_mode ranked lowest, followed in order by T_m, T₅₀H, and NPH, with the variance of NPH being as much as 100 times greater than for T_mode. These results provide guidelines for the design of experiments to generate DNA hybridization-based phylogenies and to assess their robustness with bootstrapping. Replicate drivers for a distance matrix based on T_m should use different individuals, whereas one based on T_mode could minimally use different extracts from the same individual. Thus, T_mode may be the index of choice for DNA hybridization experiments when material, time, and money are limited.Correspondence to: R. Bleiweiss     

Experimental analysis of variance for DNA hybridization: I. Accuracy

We used tissues of the Virginia opossum (Didelphis virginiana) to examine the experimental accuracy of DNA hybridization statistics of thermal stability (T_mode, T_m, T₅₀H, and NPH) with respect to systematic biases in counting radioactivity in elution fractions, and column position and loading order of hybrids in the thermal elution device. We failed to detect any change in the mean melting temperatures among five replicate ¹²⁵I-labeled hybrids counted over 72 h. Furthermore, column position in the automated thermal elution device (TED) did not bias the statistics of aliquots loaded over a few minutes from a single large mother hybrid. On the other hand, the normalized percentage hybridization (NPH) increased as much as 3–5% for aliquots loaded during 1 h from a similar mother hybrid. A parallel but less consistent increase was noted for T₅₀H, which incorporates a measure of NPH. This NPH effect disappeared when hybrids were prepared individually and diluted and loaded in turn—the usual procedure in our laboratory. Replicate distances measured as NPH appear to be sensitive to departures from the normal-distribution assumption of least-squares regression. We recommend that replicate cell values of NPH be transformed to improve their fit to a normal distribution prior to analysis by least-squares phylogenetic algorithms such as those available in Felsenstein's PHYLIP package. Thus, potential sources of inaccuracy in DNA hybridization data can be avoided with simple precautions.     

An attempt to estimate the predatory pressure exerted by the lesser weever, Trachinus vipera Cuvier, in the southern North Sea

In order to evaluate the impact of the lesser weever on the ecosystem of the southern North Sea, geographical distribution, density, growth, production and food requirements have been estimated. High densities were found on and around the Brown Ridge, an area with high tidal current velocities, medium grain-size of the sediment and a poor benthic fauna. Growth is restricted to the months of June October. During the winter cessation of growth a considerable loss of weight (about 20%) takes place. Mortality has been estimated by using the average size frequency distribution of all catches made from 1972 to 1984. The resulting convex type of survival curve indicates a high survival rate of the II to IV-group fishes. The production (estimated with Allen's graphical method) of a population of 100 individuals including all age groups (0-VI) amounts to 123.7 g AFDW-year'. In areas with highest densities, consequently, production amounts to 0.018–0.078 g AFDW-m² -year^-1. With an assumed transfer efficiency of 10% through the year, food requirements amounts to 0.18–0.78 g AFDW-m ² -year ^-1. Since the lesser weever feeds mainly on fish (85.6%), almost exclusively on gobies (Pomatoschistus sp.), and with an assumed transfer efficiency of approximately 10%, the indirect predatory pressure exerted by it may amount to 1.6 6.7g AFDW-m ².year ^-1. A possible feeding by gobies on pelagic organisms (calanoids, mysids) is discussed.     

Covariation of sexual dichromatism and plumage colours in lekking and non-lekking birds: A comparative analysis

The extreme polygyny expressed by male lekking birds leads to the expectation that sexual dimorphism should be greater in lekkers than related non-lekkers. However, evidence for this association is weak, and many lekkers are actually monomorphic in size and plumage. To better understand the kinds of plumages associated with lekking, I characterized plumage variation for combinations of sexual dichromatism and colourfulness-and-conspicuousness (COCO) among lekking and related non-lekking birds. Compared in this way, the plumages of lekkers and non-lekkers differ dramatically for both sexes. Correlations between sexual dichromatism and COCO for phylogenetically independent contrasts are significant for male lekkers (positive) and female non-lekkers (negative), but not for female lekkers or male non-lekkers. Moreover, the total number of character–state combinations, and multivariate measures of variability, are greater in non-lekkers than lekkers.The characteristic plumages of lekkers (duller monochromatic, brighter dichromatic and intermediate between these extremes) comprise just a subset of those observed among non-lekkers, and exclude extremely dull dichromatic and extremely bright monochromatic plumages. I suggest that predation, and foraging behaviours compatible with lekking, may restrict plumage variation among lekkers. Thus ecological rather than overt sexual characteristics may explain monomorphism in birds under intense mate competition, as well as the paradox of strong female mate preferences on leks, where males appear to contribute only sperm to female reproductive efforts.     

DNA hybridization evidence for the principal lineages of hummingbirds (Aves:Trochilidae)

The spectacular evolutionary radiation of hummingbirds (Trochilidae) has served as a model system for many biological studies. To begin to provide a historical context for these investigations, we generated a complete matrix of DNA hybridization distances among 26 hummingbirds and an outgroup swift (Chaetura pelagica) to determine the principal hummingbird lineages. FITCH topologies estimated from symmetrized delta TmH-C values and subjected to various validation methods (bootstrapping, weighted jackknifing, branch length significance) indicated a fundamental split between hermit (Eutoxeres aquila, Threnetes ruckeri; Phaethornithinae) and nonhermit (Trochilinae) hummingbirds, and provided strong support for six principal nonhermit clades with the following branching order: (1) a predominantly lowland group comprising caribs (Eulampis holosericeus) and relatives (Androdon aequatorialis and Heliothryx barroti) with violet-ears (Colibri coruscans) and relatives (Doryfera ludovicae); (2) an Andean-associated clade of highly polytypic taxa (Eriocnemis, Heliodoxa, and Coeligena); (3) a second endemic Andean clade (Oreotrochilus chimborazo, Aglaiocercus coelestis, and Lesbia victoriae) paired with thorntails (Popelairia conversii); (4) emeralds and relatives (Chlorostilbon mellisugus, Amazilia tzacatl, Thalurania colombica, Orthorhyncus cristatus and Campylopterus villaviscensio); (5) mountain-gems (Lampornis clemenciae and Eugenes fulgens); and (6) tiny bee-like forms (Archilochus colubris, Myrtis fanny, Acestrura mulsant, and Philodice mitchellii). Corresponding analyses on a matrix of unsymmetrized delta values gave similar support for these relationships except that the branching order of the two Andean clades (2, 3 above) was unresolved. In general, subsidiary relationships were consistent and well supported by both matrices, sometimes revealing surprising associations between forms that differ dramatically in plumage and bill morphology. Our results also reveal some basic aspects of hummingbird ecologic and morphologic evolution. For example, most of the diverse endemic Andean assemblage apparently comprises two genetically divergent clades, whereas the majority of North American hummingbirds belong a single third clade. Genetic distances separating some morphologically distinct genera (Oreotrochilus, Aglaiocercus, Lesbia; Myrtis, Acestrura, Philodice) were no greater than among congeneric (Coeligena) species, indicating that, in hummingbirds, morphological divergence does not necessarily reflect level of genetic divergence.      

Feathers with Ocular Architecture: Implications for Functional and Evolutionary Similarities of Visual Signals and Receptors

Studies of visual receptors typically assume that only functionally similar structures are relevant to the evolution of complex eyes. This approach ignores growing evidence that different functional classes of organs often share structural and developmental patterns that pertain to biological sameness (deep homology). However, the potential relevance of non-receptor structures to eye evolution remains largely unexplored. An “ocular” feather color mechanism is described whose structural and optical features resemble those of chambered, image-forming eyes to a remarkable degree. These similarities include a laterally expanded, domed light receiving surface similar to that of an eye, an encapsulated spongy tissue mass whose coherent light scattering properties in the human-visible (destructive) and ultraviolet (constructive) wavelength ranges resemble those of cornea and lens, intervening spaces such as those with humors, and a laminar pigmented shelf whose structure and optics resemble a mirrored tapetum lucidum found behind many retinas. Fourier analysis and optical principles indicate that ocular structures adhere to the same light-handling properties regardless of higher function (receptor or signal). The extent to which chambered eyes and ocular feathers have evolved independently is surprisingly equivocal. On the one hand, broad differences in the location, composition, and development of chambered eyes and ocular feather signals suggest convergent evolution on an ocular organization. However, some level of evolutionary parallelism (generative homology) between chambered eyes and ocular feathers is implicated by similarities in constructional materials, tissue development, and signal transduction cascades. Structural, optical, and developmental similarities also occur between more primitive eyes and the colored dermal papillae responsible for avian skin ornamentation. Functional constraints on light-handling requirements, coupled with developmental constraints in high-stress environments on the body surface, may enhance the similar evolutionary outcomes in the different functional setting. Regardless of the mechanistic details, repeated evolution of eye-like structures in different functional settings reveals a biological potential to produce such organs that is much greater than would be inferred from a survey of receptor structures alone.     

The allelic isozymes of hexose-6-phosphate dehydrogenase isolated from Fundulus heteroclitus: physical characteristics and kinetic properties

Hexose-6-phosphate dehydrogenase (H6PDH-A2; beta-D-glucose:NAD(P)+ oxido-reductase; E.C. 1.1.1.47) of the teleost Fundulus heteroclitus (L.) shows clinal allelic variation along the east coast of North America. Three of the major allelic isozymes have been purified and compared for native molecular weight, subunit molecular weight, isoelectric point, thermal stability, and steady-state kinetic properties (pH 8.0 and 25 degrees C). Significant differences were found among the allelic isozymes for isoelectric point, thermal stability, and some kinetic parameters. The predominant allelic isozyme in northern populations (H6PDH-AcAc) was found to be more sensitive to heat denaturation than were the predominant homozygous allelic isozymes isolated from southern populations (H6PDH-AaAa and H6PDH-AbAb). The H6PDH-AcAc allelic isozyme had both a significantly greater Km for glucose-6-phosphate than did either of the southern phenotypes and a significantly greater Km for NADP+ and Ki of NAD+ than did one of the southern phenotypes (H6PDH-AaAa). While the allelic isozymes are functionally nonequivalent, it is not yet known whether these differences are reflected at higher levels of biological organization.