Prolactin and helping in birds: has natural selection strengthened helping behavior?

The evolution of helping behavior in birds has been hotly debated.Hamilton's inclusive fitness theory has received much supportfrom ecological cost-benefit studies; however, the hypothesisthat helping has not been selected per se but is simply a phenotypicallyplastic response to altered social conditions has been proposed.In this view helping by nonbreeding birds occurs when at independencethey fail to leave their parents and are exposed to the criticalstimulus, the begging of young birds to be fed. We report thatlevels of prolactin, a hormone associated with parental behavior,are conspicuously higher in an avian species with helpers, theMexican jay (Aphelocoma ultramarina), than in a congeneric andsympatric species without helpers, the western scrub jay (A.californica). Specifically, prolactin in the nonbreeding membersof the helping species is higher than the level found in thebreeders of the congeneric nonhelping species. In addition,prolactin levels in nonbreeders rise well before the appearanceof begging young. These findings reject the phenotypic plasticityhypothesis based purely on a response to begging young and suggestthat prolactin is involved in the physiology of helping behaviorin birds as part of a complex adaptation.     

Ontogeny of Song Recognition in Birds

SYNOPSIS. This paper reviews song recognition in two congenericspecies of sparrow the swamp sparrow (Melospiza georgiana) andsong sparrow (Melospiza melodia). Data from psychophysical studiesof hearing, tutoring experiments with young birds, and fieldplayback studies with adult birds are considered together inorder to gain insight into the mechanisms of species recognitionthrough song development. In aggregate, the evidence suggestsa multi-stage process of song development consisting of an earlyperceptual preference for learning conspecific song, a sensorimotorphase of song development during which vocal output matchesan auditory memory as if through trial and error, and a finalphase of full song which functions in territorial defense andmate attraction.     

Neuromuscular Organization for "Wing" Control in a Mollusc (Clione limacina) and a Bird (Columba livia): Parallels in Design

Flapping as a means of locomotion is shared by divergent groupsranging from pteropod molluscs to birds. The pteropod, Clionelimacina, exhibits two modes of locomotion, slow and fast swimming.The motor units which control swimming consist of small motoneuronsand relatively nonfatigable muscle fibers, while those involvedin fast swimming consistof large motoneurons and relativelyfatigable fibers (Satterlie et al., 1990).The pectoralis muscleof the pigeon, Columba livia, consists of two populations ofmuscle fibers distinguished by histochemistry and size. Cinematographicand electromyographic experiments suggest that the large fibersare used for takeoff and landing and the small fibers for levelflight (Dial et al., 1988). We have employed a suite of experimentaltechniques similar to those used for studies of the neuromuscularsystem of Clione to analyze a limited sample of motor unitsfrom the pectoralis of Columba. The peak tetanic tension andcontractile fatigue resistance during electrical stimulationof single alpha axons, functionally isolated from nerve filaments,was studied in 30 motor units. All units but one generated peaktetanic tensions which were less than 0.22% of whole muscletension. A high proportion (75%) of units demonstrated fatigueresistance, reflective of the demands of sustained flappingflight. These preliminary data suggest that the peripheral neuromuscularsystems of Clione and Columba share some common components forthe execution of at least two distinct modes of flapping locomotion.     

Evolution of Eye Regression in the Cavefish Astyanax: Apoptosis and the Pax-6 Gene

SYNOPSIS. The eye is an extraordinary organ in terms of itsdevelopment and evolution. In cave animals, the eye is sometimesreduced or eliminated as a consequence of adaptation to lifein perpetual darkness. We have used the characid teleost Astyanaxmexicanus as a model system to investigate the mechanisms ofeye degeneration during the evolution of a cave vertebrate.Eyed surface populations of Astyanax entered caves during thePleistocene, and their descendants lost their eyes and pigmentation.Astyanax populations exhibiting various degrees of eye regressionhave been reported in 29 Mexican caves. Surface populationswith characteristics of the ancestral stock still exist in thevicinity of these caves. Thus, Astyanax represents one of thefew instances in which the ancestral (surface fish) and thederived (cavefish) developmental modes are extant and availablefor comparative studies. The cavefish embryo develops an opticprimordium consisting of a lens vesicle and optic cup but therudimentary eye arrests in development and degenerates. Herewe report that eye degeneration is accompanied by extensiveapoptosis and downregulation of the Pax-6 gene in the developinglens. The results suggest that alterations in lens developmentare important factors in eye regression during cavefish evolution.     

Sex allocation in response to paternal attractiveness in the zebra finch

Females mated to attractive males are predicted to produce male-biasedbroods. Previous studies on zebra finches, Taeniopygia guttata,in which colored leg rings were used to alter male attractiveness,support this hypothesis. However, because molecular sexing techniqueswere not available, it was not known when during developmentthis bias arose. Also, because both attractive (red-ringed)and unattractive (green-ringed) males were within the same aviary,assortative mating between treatments may have confounded theresults. Using two different experimental designs, we testedwhether the sex ratio of zebra finch eggs and chicks differedin response to paternal ring color whilst controlling for assortativemating between treatments. In the aviary experiment, birds couldinteract socially, but all males in an aviary had the same legring color. In the cage experiment, each female was randomlyassigned a red- or green-ringed mate, thus also eliminatingassortative mating within treatments. Offspring were sexed basedon plumage or using a molecular method. The sex ratio at layingdid not differ between treatments in either the aviary (n =313 eggs) or cage (n = 151 eggs) experiments, suggesting thatfemale zebra finches do not manipulate the primary sex ratioin response to their mate's ring color. However, in the cageexperiment we found greater male embryonic mortality in theattractive group, which resulted in a female-biased sex ratioat sexual maturity, that is, in the opposite direction to thatfound in previous studies. Possible explanations for the disparitybetween our results and those of previous studies are considered.     

Gravity-defying Behaviors: Identifying Models for Protoaves

Most current phylogenetic hypotheses based upon cladistic methodologyassert that birds are the direct descendants of derived maniraptorantheropod dinosaurs, and that the origin of avian flight necessarilydeveloped within a terrestrial context (i.e., from the "groundup"). Most theoretical aerodynamic and energetic models or chronologicallyappropriate fossil data do not support these hypotheses forthe evolution of powered flight. The more traditional modelfor the origin of flight derives birds from among small arborealearly Mesozoic archosaurs ("thecodonts"). According to thismodel, protoavian ancestors developed flight in the trees viaa series of intermediate stages, such as leaping, parachuting,gliding, and flapping. This model benefits from the assemblageof living and extinct arboreal vertebrates that engage in analogousnon-powered aerial activities using elevation as a source ofgravitational energy. Recent reports of "feathered theropods"notwithstanding, the evolution of birds from any known groupof maniraptoran theropods remains equivocal.     

Hazel grouse (Bonasa bonasia) pairs during the nonbreeding season: mutual benefits of a cooperative alliance

During the nonbreeding season (autumn and winter), hazel grouse(Bonasa bonasia) males and females associate as loosely boundpairs, not as strongly bound pairs as previously thought. Thesepairs could be considered cooperative alliances, with each membergaining both direct and indirect benefits. The most importantdirect benefit appeared to be mutual vigilance against predators.This benefit was found at two levels: at the level of arborealfeeding sites, two birds could forage faster and farther fromcover than single birds, and at the territory scale, the pairwas together more in dangerous habitats. By foraging fartherfrom cover, two birds could use about 23% more of the preferredfood trees and 9%–10% more of the food available withina territory than a single bird, partially mitigating the costof having two birds feeding on limited winter food in the samespace. Defending a common territory appeared to be a less importantdirect benefit of the alliance because the members of a pairdid not defend the same territory and often associated withneighboring birds of the opposite sex. A future benefit of thealliance was having breeding partners in the spring; this wasmost beneficial for males, as the sex ratio was male biased.Members of the pair were often apart. At arboreal feeding sites,this separation was perhaps because the most preferred trees,black alders (Alnns glutinosa) with the most staminate catkins,were located in areas with the most cover, where one bird maybe safer from predators than two. Members of pairs in more securehabitats were more often with extrapair birds of the oppositesex. This suggested a trade-off; birds in safe habitats mayhave visited potential breeding partners, but birds in dangeroushabitats may have had to remain together, foregoing this option,to increase their survival probability. This social organizationappeared to be an adaptation to surviving in a heterogeneoushabitat, with some of the winter food located in dense coverand some located in more open and dangerous situations.     

Effects of Aging and Mate Retention on Reproductive Success of Captive Female Peregrine Falcons

SYNOPSIS. Separating ecological (extrinsic) factors affectingreproduction from physiological and experiential (intrinsic)factors can be problematic in free-ranging animals. This studyexamined age-related changes in six measures of reproductivesuccess (clutch size, fertility, hatchability, brood size athatching, survivorship of nestlings, and brood size at fledging)for captive female peregrine falcons (Falco peregrinus) whereecological factors (i.e., access to mates, nesting sites, andfood) were not limiting and were similar across years and betweenindividuals. Mean nestling survivorship increased throughoutthe lifespan of the female while all other measures of reproductionpeaked at about seven years of age and decreased thereafter.Birds with prior breeding experience had higher productivitythan inexperienced birds of the same age. Productivity increasedwith increasing experience of the pair. Productivity droppedby an average of 53% when females experienced a change of mate,and then subsequently increased over a period of several years.Productivity was not affected when birds were moved to differentbreeding sites. There was no evidence that early improvementsin reproduction were related to chronological aging in the absenceof experiential differences. Birds that began breeding earlierproduced more fledglings during their lifetimes as a resultof higher annual productivity. Lifetime reproduction was notcorrelated with longevity because birds with higher maximalegg production had shorter breeding lifespans. Birds retainingmates produced more fledglings during their lifetime than birdsthat changed mates, but birds that changed mates more than oncedid not have lower lifetime reproduction than birds that hadonly one mate change. These results suggest that 1) age-relatedchanges in reproduction are not necessarily resource-mediated,2) in the absence of resource limitation, experience of thepair is a primary factor determining annual reproductive success,3) benefits of increasing experience may be offset by the onsetof senescence, 4) the cost of present egg production on futurereproductive potential supports a "pleiotropic" theory of aging,and 5) costs associated with mate changes may encourage selectionfor low "divorce" rates (i.e., lifetime monogamy) in this species.     

Conflict in the Hypaxial Musculo-Skeletal System: Documenting an Evolutionary Constraint

The identification and demonstration of an evolutionary constraintis suggested to be a four step process: 1) recognition of apossible mechanism of constraint, 2) formation of an historicalscenario of the consequences of the constraint, 3) elucidationof the causal mechanism in the modern analog or model, and 4)phylogenetic correlation of the constraint with theproposedeffect in extant lineages. Steps 1 and 2 represent the formationof two interdependenthypotheses, and steps 3 and 4 are testsof those hypotheses. This approach is illustrated with an example from the musculo-skeletalsystem of tetrapod vertebrates. Consideration of the anatomyand mode of locomotion of lizards led to the hypothesisthatthey may not be able to run and breathe at the same time. Analysisof the pattern of ventilatory airflow of lizards supports thishypothesis. Tidal and minute volume increase above resting levelsduring slow walking (i.e., speeds below 10% of maximum runningspeed), but decline rapidly at higher speeds. Furthermore, electromyographicmonitoring of the hypaxial muscles indicates a clear conflictbetween locomotor and ventilatory functions. Key anatomicalcharacters, suggested to be responsible for the conflict, canbe traced back to the earliest tetrapods. The organization ofthe two extant lineages that do breathe while running (i.e.,birds andmammals) suggests that the evolution of an abilityto breathe during locomotion required modifications of the ancestralconfiguration that separate locomotor and ventilatory function.     

Long-range Perspectives on Neurobiology and Behavior

This essay is part of the seventh presentation of a yearly educationalproject of the American Society of Zoologists. The purpose isto provide background materials for those who teach the first-yearbiology courses in colleges and universities. The Science asa Way of Knowing project emphasizes the conceptual frameworkof the biological sciences, shows how scientific informationis obtained and validated, and relates science to human concerns.The topic for consideration this year is Neurobiology and Behavior.The introductory essay is concerned mainly with the conceptualframework of neurobiology, as developed over the ages, and afew examples of behavioral studies which can be related to neurobiologyor which are of special interest through links to human considerationsand problems.     

Effect of an ectoparasite on lay date, nest-site choice, desertion, and hatching success in the great tit (Pants major)

Ectoparasites are common in most bird species, but experimentalevidence of their effects on life-history traits is scarce.We investigated experimentally the effects of the hematophagoushen flea (Ceratophyllus gallinae) on timing of reproduction,nest-site choice, nest desertion, clutch size, and hatchingsuccess in the great tit (Parus major). When great tits wereoffered a choice on their territory between an infested anda parasite-free nest-box, they chose the one without parasites.When there was no choice, the great tits in a territory containingan infested nest-box delayed laying the clutch by 11 days ascompared with the birds that were offered a parasite-free nestingopportunity. The finding that there was no difference in phenotypictraits related to dominance between the birds nesting in infestedboxes and birds nesting in parasite-free boxes suggests thatthe delay is not imposed by social dominance. Nest desertionbetween laying and shortly after hatching was significandy higherin infested nests. There was no difference between infestedand parasite-free nests in clutch size, but hatching successand hence brood size at hatching were significantly smallerin infested nests. Nest-box studies of great tits have beenseminal in the development of evolutionary, ecological, andbehavioral theory, but recently a polemic has arisen in theliterature about the validity of the conclusions drawn fromnest-box studies where the naturally occurring, detrimentalectoparasites are eliminated by the routine removal of old nestsbetween breeding seasons. Our study suggests that this criticismis valid and that the evaluation of the effects of ectoparasitesmay improve our understanding of behavioral traits, life-historytraits, or population dynamics     

Skylark optimal flight speeds for flying nowhere and somewhere

Flight is energetically very costly. For birds the mechanicalpower in relation to airspeed is characterized by a U-shapedfunction. From this function we can derive optimal flight speedsassociated with minimum power (V_mp), minimum cost of transport(V_mr) and minimum overall time of migration (V_mt). Since flightis energetically so costly, aerial displays and song flightcan potentially serve as signals reliably indicating the individualquality or resource potential of the signaler. In order to maximizethe amount of song flight produced, we expect V_mp during songflight, while during migration we rather expect V_mr or V_mv Wecompared flight speeds of skylarks (Alauda arvensis) duringsong flight and migration flight, respectively. In this speciespredicted V_mp = 5.5 m/s, V_mr = 10.5 m/s, and V_mt = 12.1 m/s.The preferred airspeed during song flight did not differ significantlyfrom the predicted V_mp, while airspeed during migration wassignificantly higher than V_mr and Vmp indicating that flightspeed is a flexible trait that birds adjust to different situations.Why the skylarks speed up so much on migration is still unclear,but it may be that due to the shape of the predicted power curve,variation in cost of transport at high speeds is relativelysmall.     

Immunoparasitology in Avian Species

There has been no work on the immunological response of birdsto helminth infections since the late 1960s, an area of investigationthat has been too long ignored. Similarly, studies of arthropod-mediatedresponses in birds are lacking except for a few scattered investigations.Recently, a serum antibody response has been seen against onearthropod, the northern fowl mite. The appearance of antibodiesrecognizing an 8–10 kilodalton mite antigen seems to correlatewith a reduction in the mite population on infested chickens.Most of the studies on parasite immunity in avian species havecentered on the economically important Eimeria species, protozoanparasites that infect the intestine of chickens and turkeys.These investigations encompass wide areas of interest includingthe effect of immunity on parasite invasion, development ofT-cell proliferation assays and T-cell clones, inhibition ofparasite penetration and development by hybridoma antibody treatment,production of genetically engineered Eimeria antigens used inbird immunization studies, and studies using inbred or congeniclines of birds to determine what effect the major histocompatibilitycomplex has on parasite immunity. From these efforts it hasbeen learned that not only is the immunity species-specific,but also depending on where in the intestine the parasite invades,penetration is either not affected or inhibited by as much as50%. The T-cell proliferation assays suggest that this specificitymay be due to a species-specific T-cell response. Immunizationstudies using a genetically engineered antigen have indicatedthat at least partial protection against one species of Eimeriais possible. Studies done with the inbred congenic lines ofbirds have shown that the genetic makeup of the bird is importantin how it responds to either a natural infection or to immunizationwith a genetically engineered antigen. Clearly, these resultsshow not only the complexity of the bird response to parasiteinfection, but also the amount of work still undone.     

The Expression of Beta ({beta}) Keratins in the Epidermal Appendages of Reptiles and Birds

The integuments of extant vertebrates display a variety of epidermalappendages whose patterns, morphology and terminal differentiation(epidermal keratins) depend upon interactions between ectodermal(epidermis) and mesodermal (dermis) tissues. In reptiles andbirds, appendage morphogenesis precedes terminal differentiation.Studies have demonstrated that appendage morphogenesis influencesthe expression of the appendage specific keratin genes. However,little is known about the nature of the structural genes expressedby the epidermal appendages of reptiles. How pattern formationand/or appendage morphogenesis influence terminal differentiationof reptilian appendages is not known. The epidermal appendages of reptiles and birds are characterizedby the presence of both alpha () and beta (ß) typekeratin proteins. Studies have focused on the genes of avianß keratins because they are the major structural proteinsof feathers. The occurrence of ß keratin proteinsin the scales and claws of both birds and reptiles and theirimmunological cross-reactivity suggest that the genes for reptilianß keratins may be homologous with those of birds.In bird appendages, the ß keratins are the productsof a large family of homologous genes. Specific members of thisgene family are expressed during the development of each appendage.Recent sequence analyses of feather ß keratins, fromdifferent orders of birds, demonstrate that there is more diversityat the DNA level than was implied by earlier protein sequencingstudies. Immunological techniques show that the same antibodies thatreact with the epidermal ß keratins of the chicken(Gallus domesticus) react with the epidermal ß keratinsof American alligators (Alligator mississippiensis). Furthermore,a peptide sequence (20 amino acids) from an alligator claw ßkeratin is similar to a highly conserved region of avian claw,scale, feather, and feather-like ß keratins. Theseobservations suggest that the ß keratin genes of avianepidermal appendages have homologues in the American alligator.Understanding the origin and evolution of the ß keratingene families in reptiles and birds will undoubtedly add toour understanding of the evolution of skin appendages such asscales and feathers.     

Bird-pollinated flowers in an evolutionary and molecular context

Evolutionary shifts to bird pollination (ornithophily) haveoccurred independently in many lineages of flowering plants.This shift affects many floral features, particularly thoseresponsible for the attraction of birds, deterrence of illegitimateflower visitors (particularly bees), protection from vigorousforaging by birds, and accurate placement of pollen on bird'sbodies. Red coloration appears to play a major role in bothbee-deterrence and bird-attraction. Other mechanisms of bird-attractioninclude the production of abundant dilute nectar and the provisionof secondary perches (for non-hovering birds). As a result ofselection for similar phenotypic traits in unrelated bird-pollinatedspecies, a floral syndrome of ornithophily can be recognized,and this review surveys the component floral traits. The strongconvergent evolution evident in bird-pollinated flowers raisesa question about the nature of the genetic mechanisms underlyingsuch transitions and whether the same gene systems are involvedin most cases. As yet there is too little information to answerthis question. However, some promising model systems have beendeveloped that include closely related bee and bird-pollinatedflowers, such as Ipomoea, Mimulus, and Lotus. Recent studiesof floral developmental genetics have identified numerous genesimportant in the development of the floral phenotype, whichare also potential candidates for involvement in shifts betweenbee-pollination and bird pollination. As more whole-genome informationbecomes available, progress should be rapid. Key words: Anthocyanin pigmentation, bird-pollination, candidate gene, developmental genetics, honey-eaters, hummingbirds, nectar, ornithophily, pollination syndrome, sunbirds Received 2 November 2007; Revised 21 December 2007 Accepted 7 January 2008     

A View of Comparative Endocrinology and Aubrey Gorbman

Analyses of papers published in General and Comparative Endocrinologyfrom 1961 to 1981 were made from several aspects. Number ofpapers published has increased year after year. Molluscan endocrinologypapers have increased and overtaken annelid publications. Duringthe past 20 yr studies using crustaceans and insects have comprised25–50% of all endocrine research on invertebrate groups.Papers on protochordates, elasmobranchs, and cyclostomes arefew but constant in number, indicating that these three groupsare important from phylogenic aspects. Studies on birds andteleosts have increased, while those on amphibians have decreased.Biochemical techniques were employed in 50% of all publicationsin this journal. Radioimmunoassay has replaced autoradiography.Immunohistochemistry increased in popularity. Studies on thepars distalis and gonads are predominant among all endocrineorgans. Research at the molecular level is decreasing, but isincreasing at the organismal level. Research at the organismallevel may be characteristic of comparative endocrinology. Largelythrough the initiative of Aubrey Gorbman, General and ComparativeEndocrinology was first published in 1961, and the InternationalCommittee of the Symposium on Comparative Endocrinology wasformed in 1957. Gorbman has produced many students. His originaland important contributions are in diversified areas: thyroidphysiology and its evolution, hormones and the brain and behavior,cyclostome endocrinology and neurosecretory systems in lowervertebrates. In addition, he has influenced investigators throughhis ideas of evolution. He has had particular impact on thedevelopment of comparative endocrinology in Japan.     

DOES TANDONIA BUDAPESTENIS (MOLLUSCA: PULMONATA) CONTAIN TOXINS? EVIDENCE FROM FEEDING TRIALS WITH THE SLUG PREDATOR PTEROSTICHUS MELANARIUS (COLEOPTERA: CARABIDAE)

Slugs are known to be killed and consumed by a range of invertebrateand vertebrate predators in the field. Carabid beetles (Coleoptera:Carabidae) in particular are major natural enemies of slugs,and have been shown to be capable of controlling certain speciesin a crop environment. This paper reports experiments to investigatethe effects, on the carabid Pterostichus melanarius, of feedingon the milacid slug Tandonia budapestensis. The slugs provedto be toxic, 50% of the beetles dying within two days. Mortalityof beetles fed on two other species of slug, Deroceras reticulatumand Arion distinctus, was not significantly different from thatfor beetles fed upon a control prey (Calliphora vomitoria).These results represent the only known case of a European slugproving to be toxic to potential predators, and is one of avery small number of reported instances of possible toxicityamongst terrestrial gastropods. The possibility that the orangeline down the dorsal keel of T. budapestensis may act as warningcoloration to birds is discussed. (Received 4 December 1996; accepted 5 March 1997)     

A Brief Review of Metazoan Phylogeny and Future Prospects in Hox-Research

Underlying any analysis on the evolution of development is aphylogenetic framework, whether explicitly stated or implied.As such, differing views on phylogenetic relationships leadto variable interpretations of how developmental mechanismshave changed through time. Over the past decade, many long-standinghypotheses about animal evolution have been questioned causingsubstantial changes in the assumed phylogenetic framework underlyingcomparative developmental studies. Current hypotheses aboutearly metazoan history suggest that three, not two, major lineagesof bilateral animals originated in the Precambrian: the Deuterostomes(e.g., seastars, acorn worms, and vertebrates), the Ecdysozoans(e.g., nematodes and arthropods), and the Lophotrochozoans (e.g.,annelids, mollusks, and lophophorates). Although informationin Hox-genes bears directly on our understanding of early metazoanevolution and the formation of body plans, research effort hasbeen focused primarily on two taxa, insects and vertebrates.By sampling a greater diversity of metazoan taxa and takingadvantage of biotechnological advances in genomics, we willnot only learn more about metazoan phylogeny, but will alsogain valuable insight as to the key evolutionary forces thatestablished and maintained metazoan bauplans.     

Peripheral Thyroid Hormone Dynamics in Precocial and Altricial Avian Development1

SYNOPSIS. Precocial and altricial birds have distinctly differentpatterns of general ontogeny and metabolic/thermoregulatorydevelopment. In my laboratory, we have studied the developmentof thyroid function in Japanese quail (Coturnix japonica) andRing doves (Streptopelia risoria) as examples of precocial andaltricial development, respectively. In this paper, I reviewthe literature and our work on the factors that influence peripheralhormone dynamics in birds. The first section of the paper describesadult peripheral thyroid function to set the stage for the developmentalpicture. Thyroid development is divided into two phases: PhaseI, in which the thyroid gland develops functional capacity butthere is low thyroid activity in the periphery, and Phase II,in which peripheral thyroid function increases and approachesadult levels. In precocial development Phase I occurs duringembryonic life and Phase II begins at the perinatal period.In altricial development, the pattern of thyroid functionaldevelopment is different and delayed. Peripheral thyroid hormonepatterns in both developmental modes are discussed with referenceto the factors that determine their dynamics: hormone availabilityfrom the thyroid gland, total serum hormone concentrations,the roles of serum binding proteins in regulating freehormoneconcentrations, hormone turnover and excretion, hormone receptorsand thyroid hormone metabolism, especially extrathyroidal productionof triiodothyronine from thyroxine.