And now for something completely different....
No, it's not a quest featuring mysterious riddles. Nor is it a rogue pootie diary. It's real actual bird science. I'm going to (ab)use my Dawn Chorus guest privileges this week to talk about behavioral and evolutionary research relating to our feathered friends. Because this is a community diary I'm going to try and keep it light and cordon off the gritty details so that they doesn't harm innocent bystanders. I'm also supplying pictures/video off the web and some background on the species involved. If you have any questions feel free to ask. Or if you want to talk about something completely different that's cool too.
This diary is really, really long. So I've split it into three major sections, each of which is self-contained so you can look at the one that catches your fancy and not waste your entire Sunday. One is on mate choice and the evolution of bright colors and displays. The second is on the evolution of aging and the third is on how the use of molecular information has transformed our knowledge of evolution. Within each section I'll give a bit of background and talk about some interesting recent science on birds (and a few other things). The title of each study is given in ALL CAPS so that you can easily skip down to the next one if you get bored. I'll follow with a brief overview. In a few cases I'll give more detail (for those interested) in italics (so you know what to ignore). Those of you who just want the gist of the outcome can skip down to where I've written PAYOFF in all caps and not worry about any of the details.
I. Bright Feathers, Sweet Songs and Wacky Dances: The Evolution of Mate Choice
Among the characteristics that attract us to birds are their bright colours and pleasant songs. These traits are the product of sexual selection. Sexual selection was an idea of Darwin's he developed to explain traits such as the peacock's tail which are not used in rearing offspring and are probably a hindrance to survival. Mate choice is one of the two forms of sexual selection. A really hot topic over the last 3-4 decades has been the evolution of mating preferences.
Photo by the author. Taken in Urbana, Illinois
Tom Turkeys have this big fan tail, a naked blue head, red wattle and wacky little thing-a-ma-bob coming out of their chest. They also have a fleshy snood that covers their beak. Female turkeys apparently prefer to mate with males with longer snoods. They may also make mating decisions based the other odd ornaments that males have. Bu why? Why should an individual base mating decisions on these apparently useless characteristics?
One idea that has attracted a lot of attention is condition dependence. Traits like bright colors often vary with the health and vigor of the animal. So a female may be able to assess a prospective mate's health and potential to carry out his paternal duties by checking out the brightness of his plumage. She might also be able to assess how resistant a potential mate is to disease, a trait that could be passed along to her offspring. Apparently the length of the snood is associated with certain types of parasitic infection.
A MULTIFACTORIAL TEST OF THE EFFECTS OF CAROTENOID ACCESSS, FOOD INTAKE, AND PARASITE LOAD ON THE PRODUCTION OF ORNAMENTAL FEATHERS AND BILL COLORATION IN AMERICAN GOLDFINCHES.
Hill, G.E. et al. 2009. The Journal of Experimental Biology 212, 1225-1233
Photo from Wikimedia Commons, taken by Mdf at Rondeau Provincial Park, Ontario, Canada.
This may not seem like a very exciting study at first glance but it is a good example of a large scale study looking at multiple factors at once - something that is difficult to do in birds. The goal is to tease apart the relative importance of several environmental factors on different aspects of bird colouration.
A lot of work on condition dependent traits has been done with House Sparrows, House Finches, and Goldfinches. These birds are all common and don't take up as much space as turkeys. They also have male-specific color patterns that may be involved in mate choice. Bird colors can be derived from pigments or they can be structural. Two major sources of pigments are melanin and carotenoids. Melanin can be made by animals from amino acids and is less dependent on specific foods. In contrast these finches cannot make carotenoids (although they can modify them) and they need to get them directly from foods they eat. Carotenoids are responsible for most yellow/red coloration.
The role of disease and parasitism in mate choice was first postulated almost thirty years ago in what is known as the Hamilton-Zuk hypothesis. The idea is a bit complicated. A problem with the idea that females select males based on genetic quality is that the end result would be genetic uniformity (if only the genetically 'best' males mate then rapidly all the individuals in the population would have those 'best' genes). Disease organisms and their hosts continuously evolve in response to one another so genetic 'quality' with regard to disease resistance is a moving target.
A lot of studies have found that food availability, the amount of parasites, and direct access to carotenoids have major affects on male coloration and their attractiveness to females. Usually these studies have looked at one factor at a time. In this study all three factors were varied simultaneously. Mate choice was not tested in this study but has been tested by the authors in other work.
PAYOFF: The black caps of goldfinch (a melanin based pigment) was not affected by diet, carotenoids, or parasites. The yellow pigment was affected by supplemental carotenoids but not by food access or parasites. The color of the male beak was affected by all three factors. The interesting part of this is that the beak and yellow feather traits don't seem to respond in the same way. The authors' interpretation is that the two things are sending different signals about a male's condition.
MATE CHOICE FOR GENETIC QUALITY: A TEST OF THE HETEROZYGOSITY AND COMPATIBILITY HYPOTHESES IN A LEK-BREEDING BIRD.
Ryder, T.B. et al. 2010. Behavioral Ecology (volume #?) 203-210.
Now we are getting to some really wild stuff. This study was done on Wire-Tailed Manakins in Ecuador.
Here is a video of a Wire-Tailed Manakin sitting around. You can see they are pretty amazing looking birds
Follow this link to see a fantastic video of one displaying. Normally they don't have a soundtrack.
Manakins are doubly interesting because the displaying is done in a lek. A lek is an area in which a number of individuals of one sex (usually males) gather. Each male defends a tiny space within the lek and displays there. Females visit the lek to mate and then leave to lay eggs and rear offspring on their own. Probably the most well known North American bird to have leks is the Sage Grouse.
The factors leading to lek evolution are not well understood. However lekking animals have been great for studying sexual selection because mate choice appears to be driven only by male coloration and display. Unlike many if not most other birds species the male does not care for the offspring and does not even defend a territory in which the female can nest. The only contribution made by males are their genes.
One possible reason for genetic based mate choice is to avoid producing offspring that are too genetically uniform. We have two copies of each gene in our genome. If the two copies are the same - that is homozygous (e.g. two copies of the gene for blue eyes). If the two copies are different (e.g. one copy for blue eyes and one for brown eyes) that is heterozygous. Greater genetic diversity, particularly for genes associated with the immune system is usually beneficial. There is considerable evidence that individuals often select mates that are genetically dissimilar to themselves.
PAYOFF: This study found that female manakins did not select genetically more dissimilar mates at the leks, in facts mated pairs were more closely related to one another than would be expected by random chance. However males that were more heterozygous were more successful at getting mates. More heterozygous males also had bigger wings and shorter legs than less heterozygous males. It appears the success of highly heterozygous males has more to do with competition among males rather than mate choice. The authors conclude that the fact that females are mating with relatives is linked to the population structure of manakins.
A Mormon Cricket From Wikimedia Commons - in the public domain
OK - I'm going to say that I simplified some things up at the start. Darwin phrased his ideas about sexual selection in terms of competition among males and female choice of mates. This is a common pattern and there are good reasons why it should be so. However it is a bit too simplistic. There are quite a lot of animals in which the roles are reversed. A classic example is the Mormon Cricket (which is actually a type of katydid). When they mate males transfer sperm in a packet called a spermatophore. Attached to this packet is a nutrient rich mass called the spermatophylax. In quite a few insect species the female feeds on this spermatophylax while the sperm leave the spermatophore and enter her reproductive tract.
Male mormon crickets produce giant spermatophylaxes, up to one third of their body weight. So each time a female mates she gets a huge meal. Each time a male mates he needs to produce a new spermatophylax, which can take several days. In this species females are eager to mate as often as possible while males are extremely choosy about mating, generally only selecting the largest available females as mates.
Which leads us to...
THE ECOLOGICAL BASIS OF UNUSUAL SEX ROLES IN REVERSE-DICHROMATIC ECLECTUS PARROTS.
Heinsohn, R. 2008. ANIMAL BEHAVIOUR, 76, 97-103
Photo from Wikimedia Commons. Taken by Doug Janson at the Singapore Zoo.
Above are a female (right) and male (left) Eclectus parrot. My wife and I first saw these at the St. Louis Zoo some years ago and right away realized that something evolutionarily interesting might be going here. A typical pattern you see in birds is to have a brightly coloured male and a less brightly coloured female (e.g. Cardinal). Also fairly commonly you will see examples of species where both the females and males have the same bright colours (e.g. Macaws or Jays). More rarely you see examples where the females are brightly coloured and the males are dull (e.g. Phalaropes). I don't know of any other bird where the males and females are brightly coloured but have completely different colour patterns.
And now it turns out that there has been this major field study of Eclectus parrots in northern Australia. Here are a couple of videos of the birds in the field and data collection. Female Eclectus compete with each other for nesting cavities. Apparently the quality of the cavities is highly variable and getting a good one is primo. Females remain in the cavities for eleven months a year and are fed by males. The male bright green color is thought to have evolved through female choosiness (females have the opportunity to mate with multiple males while staying at their nest) while the female color is thought to have evolved through competition between females for the best nesting cavities. This is a very challenging bird to study as they nest very high in trees in remote regions. So at this stage we have intriguing explanations but I don't think they have been conclusively tested.
Both photos from Wikimedia Commons. Upper photo by Jurgen Schiller Garcia at the Frankfur Zoo, photo modified by Snowmanradio. Lower photo by Martin Pot at unknown location.
SEX CHROMOSOME LINKAGE OF MATE PREFERENCE AND COLOR SIGNAL MAINTAINS ASSORTATIVE MATING BETWEEN INTERBREEDING FINCH MORPHS
Pryke, S.R. 2010. Evolution 64:1301-1310.
Gouldian finches live in Australia. The pictures above show two male. Obviously they are different colours. In the wild males exist in these two colour forms (morphs). In captivity a number of other colour forms have been produced. The existence of the two morphs is interesting because if females choose mates based on colour then you would expect one of the two forms to preferred over the other and to eventually win out.
The answer to the question is equally interesting. It turns out that the genes for the color and the genes for the female preference are both on the Z sex chromosome*. So a mated pair will tend to consist of a male of a morph and a female that prefers that morph. Any daughters of the pair will inherit their mother's preference and any sons their father's trait. In the wild there is any interbreeding between the two groups to keep them from separating into two species but the genetic linkage between male color and female preference maintains both colour forms in the population.
*Birds have a different system of sex chromosomes than humans. Humans, and all other mammals except the Platypus, have an XY system where females have two X chromosomes and males have an X and a Y. The presence of a Y makes you male, if there is no Y then you are female. In birds males have two Z chromosomes and females have a Z and a W. The W makes you female, no W means you are a male.
Photo by the author. Female Weta near Wellington, New Zealand
SEXUAL SELECTION FOR MALE MOBILITY IN A A GIANT INSECT WITH FEMALE-BIASED SIZE DIMORPHISM
Kelly, C.D. et al. 2008. The American Naturalist 172:417-422.
I threw this last one in for two reasons. One, I think Wetas are really cool. Two, it illustrates an important point. A lot of studies of sexual selection focus on the spectacular and the bizarre. Most of the time sexual selection is acting on much more mundane characteristics.
Wetas are giant relatives of crickets and grasshoppers found in New Zealand. Females are much larger than males. Having female be larger than males is actually quite common - the usual explanation is that larger females can produce more eggs while there is no such relation between male size and sperm production. In the case of the Wetas the size difference is extreme with females being many times the size of males. The authors hypothesized that, like in some spiders, the small size of males may make them more agile and be quicker in finding and mating females. In other words this contest is about speed rather than strength or beauty. Their results did indicate that males with smaller bodies and longer legs travel further and faster and are more successful in inseminating females.
II. Live fast, die young? The Evolution of Aging
Earlier this week, when I told lineatus that I was going to talk about aging in birds she said that was her 'favorite topic bar none.' I realized later that she might be thinking of something a bit different from what I had in mind. I'm going to talk about evolutionary theories of aging and how research on birds has played a role in this field. And I'll cap it off with a cool recent paper on albatrosses. Our friend below reminds us that all of what I'm going to discuss depends on actually knowing how old birds are, which is not trivial.
Photo and caption by lineatus. Used by invitation.
Why do organisms age? This is a really fascinating question with a fairly complex answer.
Senescence is the decline in physiological performance of organisms over time. Many biologists have interpreted this as a fundamental property of biological systems Things break down - it's just entropy. But why do different species age at such different rates? A mouse is ancient at two years of age, while at the same age a cat is a young adult, and a human is still an infant. Physiologists noted that larger animals tended to live longer than smaller animals (e.g. an elephant lives longer than a horse which lives longer than a dog) as shown in the graph below for birds and mammals. Size is related to metabolic rate - larger animals have slower metabolic rates than do smaller animals. The physiologists hypothesized that animals with faster metabolisms would 'burn out' faster and hence have shorter lifespans.
Evolutionary biologists have come up with an alternative theory (actually two similar theories but I'll ignore that) in which physiological lifespan evolves due to differences among species in what I will call ecological lifespan. Most individual organisms in the wild never live long enough to experience aging. 'Nature red in tooth and claw' means that an animal's chances of ending up as someone's lunch before it ever get the chance to feel the pangs of old age are pretty high.
Now comes the tricky bit. The strength of natural selection declines as organisms age. A trait that helps a juvenile harrier survive to the age of two years when it can breed is going to be under strong selection. A trait that doesn't kick in until the bird is say 12 years old is going to be under much weaker selection because very few birds will live to be that old and the contribution to the next generation by birds of this age is going to be very small.
So genes that have good effects early in life are going to be under strong and positive natural selection while genes with bad effects at ages when the animal is unlikely to be alive for ecological reasons are going to be under very weak negative natural selection. So genes with bad effects later in life will persist and they will have effects at earlier ages for species that are more likely to die young in the wild.
The graph above illustrates how this might work. We have survivorship curves for three lizard species (I couldn't find a bird example). Each curve starts with 1000 hatchling lizards and shows how many of the 1000 are still alive at different ages. For the Xantusia over half are still alive at age 3 and about a third at age 6. This means that a substantial proportion of the population will consist of animals of these ages and natural selection will act to remove genes that have bad effects at those ages. In contrast the Sceloporus are virtually all dead by age 3 so any genes that have bad effects at later ages will be under no negative natural selection.
Now we get to the bird part. The evolutionary hypothesis makes the same prediction for body size and physiological lifespan that the physiological hypothesis did but for a different reason. Larger animals should live longer, not because they have a lower metabolic rate but because they are safer from predation. But when you compare birds and mammals you get different predictions for the two hypotheses.
Birds have the same pattern as mammals for physiological lifespan - larger bird species tend to live longer than smaller bird species. However for any given body size birds tend to live significantly longer than mammals (compare the blue and red dots on the graph above). Larger parrot and seabird species have lifespans similar to elephants for example. This is opposite to the prediction of the physiological hypothesis as birds have higher metabolic rates than mammals (it takes a lot of energy to fly) but it fits in with the evolutionary hypothesis (flight probably keeps birds safer from predators). A couple of other observations further support the evolutionary hypothesis: 1. bird species that are long distance migrants have shorter lifespans than non-migratory birds, reflecting the greater hazards of migration; 2) bats have lifespans similar to birds of the same size.
Photo from Wikimedia Commons. Taken by Steve Jurvetson at Menlo Park, CA
EVOLUTION OF SENESCENCE IN NATURE: PHYSIOLOGICAL EVOLUTION IN POPULATIONS OF GARTER SNAKES WITH DIVERGENT LIFE HISTORIES.
Kylie, R.A. and Bronikowski, A.M. 2009. The American Naturalist 107: 147-159.
OK we're going to diverge from birds for a moment. There has been a lot of experimental work (mostly on fruit flies which have the advantage of not living very long) that has tended to back up the evolutionary hypothesis I described above. This garter snake study combines field derived information with a lab experiment. The species is the Wandering Garter Snake which is found broadly over the west of North America. The picture is of the coastal subspecies. This study involves two different populations of the inland subspecies. Both populations occur in the vicinity of Eagle Lake in northeastern California.
The Lakeshore population suffers a high death rate due to bird predation. In contrast the Meadow population has a very low death rate. Lakeshore snakes invest heavily in offspring (lots of babies) and don't live very long while the Meadow snakes have fewer young per year and live much longer. This study looks at a variety of physiological characteristics of the young snakes born in the lab (so the differences are not likely to be the result of the environment). Among the differences they found were much faster DNA repair after UV damage in the Meadow snakes and a greater resistance to oxidative damage during cellular respiration (thought to be a major component of aging). So the lakeshore snakes are really following Neil Young's lyrics - 'better to burn out than to fade away' while the meadow snakes are better at not rusting.
For some time it was thought that senescence (physiological aging) was something that was rarely seen in the wild - that most animals would die before getting old enough to show signs of aging. This is true but for long-lived species it is now known that a significant number of individuals do show senescence in the wild. Such as Wandering Albatrosses.
Photo by the author. Taken offshore from Kaikoura, New Zealand
PATTERNS OF AGING IN THE LONG-LIVED WANDERING ALBATROSS.
Lecomte, V.J. et al. 2010. Proceedings of the National Academy of Science 107:6370–6375
The bird in the middle of the above shot is a Wandering Albatross. They are among the largest of flying birds and can live to at least 60 years of age. When they first fledge they are brown all over and over the first several years of their lives they lose the brown on their bodies and (more slowly) on their heads. As adults the dark colouration is largely confined to the upper surface of the wing (this varies a bit depending on the geographic race of Wanderer). Gradually as the birds age the dark is replaced by white in a piece meal fashion (as you can see in the photo). Old males of the south Atlantic/Indian ocean populations may be virtually pure white.
French researchers have been carrying out a long term study of Wandering Albatrosses breeding on the Crozet Islands in the southern Indian Ocean. These birds start breeding at age seven and they have banded birds of known ages up to 47 years. They measured physiological parameters, reproductive success, and foraging behavior and success (using radio/satellite telemetry) to look for signs of aging.
The found that age had no effect on any of the physiological factors they measured but that older birds were less successful in fledging chicks. The most striking finding is illustrated below.
Females of all ages foraged in the same general area throughout their lives. Males less than 25 years old foraged in the same general area as females while males over the age of 25 foraged further south in Antarctic waters. Older males also spent more time on the surface of the water and returned to the colony with elevated levels of stress hormones.
They were kind of baffled by this change in foraging pattern but came up with two possible explanations. 1) older males are finding foraging more stressful and therefore sit on the surface more to rest. The high winds of the Antarctic make flying and take off less energetically expensive. 2) The difference is not real but results from a small sample size.
III. What We Can Learn From Molecules
This section is going to focus more on techniques. The research questions, while interesting, are fairly simple because I want to convey how the techniques of molecular biology have helped expand our knowledge of evolution (and even ecology).
CONTRASTING PHYLOGEOGRAPHIC PATTERNS IN MITOCHONDRIAL DNA AND MICROSATELLITES: EVIDENCE OF FEMALE PHILOPATRY AND MALE-BIASED GENE FLOW AMONG REGIONAL POPULATIONS OF THE BLUE-AND-YELLOW MACAW (PSITTACIFORMES: ARA ARARAUNA) IN BRAZIL
by Capparoz et al. 2009. The Auk 126:359-370.
Let's start out by learning about blue and yellow macaws, by way of a tribute to lineatus' beloved Amelia. You might think a three foot long, bright blue and yellow and incredibly noisy bird would be easy to follow. However, parrots spend a lot of time in and above the canopy of tropical forests and they are rapid fliers. I would imagine they are also very difficult to catch for banding/tracking purposes. So to learn a bit about their population structure and evolutionary history its molecules to the rescue!
Photo from Wikimedia Commons. Taken by Tony Brierton at Pont-Scorff Zoo, Morbihan, Brittany, France.
In this study blood and tissue samples were taken from birds across Brazil (either chicks in the nest or locally caught adults. Selected portions of the birds' genetic material were sequenced. Specifically the geographic pattern of variation in the mitochondrial DNA was compared to geographic variation in DNA sequences from the rest of the genome. Why do this and what the heck is mitochondrial DNA? As you may remember from high school bio, the mitochondrion is the 'powerhouse of the cell'. They are the descendants of ancient bacteria that moved into our ancestors' cells a couple billion years ago and they still have a small amount of their own DNA. Mitochondria are passed from parents to offspring in eggs but not through sperm. So all of your mitochondria are descended from ones you got from your mother.
This gives mitochondrial DNA a couple of useful properties. It doesn't get mixed in with all the other DNA during sexual reproduction and thus changes much more slowly over evolutionary time. And it is only passed down through the female line allowing some interesting comparisons. In this case they found that macaws in western Brazil had clearly different mitochondrial DNA sequences than did those in the east. The extent of the sequence differences indicated that the mitochondria in the west and the east had been separated for about 375,000 years. But when they looked at other DNA sequences they found no differences between the macaw populations in the east and in the west.
PAYOFF: The molecular evidence demonstrates three things about the Brazilian blue and yellow macaws. 1) They were geographically separated into two areas about 375,000 years probably by climate change. 2) Individuals move back and forth between the two areas often enough to keep them genetically similar. 3) The fact that the mitochondrial DNA is not similar indicates that it is males doing the moving. This is the interesting bit. In most birds it is the females that move away and males live close to where they were born (or return to close to where they were born if they're migratory). Macaws appear to have the more mammal typical of male departure with females remaining near the area of their birth.
LOCAL ADAPTATION MAINTAINS CLINAL VARIATION IN MELANIN-BASED COLORATION
OF EUROPEAN BARN OWLS (TYTO ALBA)
by Antoniazza, S et al. 2010. Evolution 64: 1944–1954
Barn Owls have one of the largest geographic ranges of any terrestrial animal (not counting ones moved by humans). They are found on all continents. Over their range they exhibit a wide range of colouration. In this study DNA sequences were compared from owls from different areas of Europe. The colouration of the owls in different areas was also compared.
Photo from Wikimedia Commons. Taken by HeBi in the Netherlands. These Owls represent two different geographic forms.
The question of interest here is the extent to which colour variation is the result of natural selection (i.e. the colour represents an adaptation to the local environment). An alternative explanation is that the colour variation is largely due to random changes in each population accumulating over time.
To test this they used DNA (as was the case in the first study) sequences that don't code for anything. Our cells have lots of this DNA which essentially does nothing except make copies of itself. Because it doesn't do anything it is not subject to natural selection and and differences among populations are thought to be random changes over time.
What was found was that there was very little difference in the non-coding DNA sequences among the different populations of Barn Owls. This indicates that owls move between populations often enough to wipe out differences that have arisen through chance.
PAYOFF: Because the colour differences among the populations persist despite the high rate of owl movement (revealed by the DNA sequences) among those same populations the idea that these differences are maintained by natural selection is supported. The different colours represent adaptations to the local environment.
HISTORICAL DIVERGENCE AND GENE FLOW: COALESCENT ANALYSES OF MITOCHONDRIAL,
AUTOSOMAL AND SEX-LINKED LOCI IN PASSERINA BUNTINGS
by Carling, M.D. et al. 2010. 64: 1762–1772
Photos from Wikimedia Commons. Upper Photo of Indigo Bunting by Kevin Bolton, location unknown, Lower photo of Lazuli Bunting taken in Oregon and is in the Public Domain.
Here's a more complicated question and I'm going to skip over pretty much all the technical details. Indigo and Lazuli Bunting are two closely related species that live in eastern and western North America respectively. Apparently the two species interbreed (hybridize) where they come into contact in the center of continent.
Based on historical data the two species have been in contact for at least 120 years. The earliest date they could have come into contact is about 6,500 years ago based on knowledge of the climate and environment in the past.
Prior to that time the two species were geographically separated from one another. The question is whether that separation was complete or if there was some contact and interbreeding over their evolutionary history. It is much harder for one species to split into two if there is not complete isolation for some period.
PAYOFF: Using techniques similar to, but more complicated than, those in the two studies immediately above the researchers found that the two species formed from an ancestral species at least one million years ago (different techniques gave different estimates) and there had been interbreeding since that time. This indicates that either the two populations had never been completely separated or that there was contact from time to time between the separated species.
The genetic data find that there is much less mixing of mitochondrial genes and genes on the sex (Z) chromosomes than in the rest of the genome. This is consistent with what is known as Haldane's Rule. This rule states that if hybrids between two species are less healthy and fertile the effect will be seen most strongly in the sex with two different sex chromosomes. In birds that sex is female (ZW) while males have two Z chromosomes. The data are consistent with female hybrids being much more likely to die or not breed than male hybrids.