MBNA Rose Center VISA
     


June 2002

Avian Quick-Change Artists

Exemplars of rapid adaptation, house finches show that mothers know best.

By Alexander V. Badyaev and Geoffrey E. Hill

Avian Quick-Change Artists

Adaptation to the environment is the cornerstone of Darwinian natural selection. Among the most conspicuous consequences of this process are changes in the size and shape of animals in response to climate. Nearly 200 years ago, long before the publication of Darwin's Origin of Species, zoologists recognized that in wide-ranging species, individuals that inhabit the colder parts of the range tend to be larger and to have shorter limbs and appendages (black bears and white-tailed deer, for example, show this trend in North America). When one is considering species that have had stable ranges over thousands of years, such changes in body size and shape can be assumed to have evolved very slowly, by incremental stages, over many thousands of generations. Biologists only rarely have a chance to witness the pace of such changes when a population of vertebrates spreads into a very new environment. Over the past few years, however, we have documented rapid and adaptive changes in the size and shape of one vertebrate species—the house finch—and we have discovered a fascinating and unanticipated mechanism that allows this bird to adjust quickly to local environments.

House finches were originally found only in western North America. When northern Europeans first settled on the East Coast and the Spanish colonized the Southwest, these sparrowlike birds ranged from Oregon and Wyoming to southern Mexico and east to the foothills of the Rocky Mountains. Originally birds of open savannas, canyons, and deserts, house finches avoided both forested and treeless regions; the Great Plains and the dense forests of the Pacific Northwest were unsuitable habitat for them. Eventually, unbroken woodlands were felled to make way for farms and cities, and in the process, huge new areas suitable to house finches emerged. In response, they expanded their range, eventually spreading to British Columbia and western Montana by the 1980s.  In the eastern United States, humans lent a hand in establishing house finch populations (see "Hollywood, Honolulu, and Hoboken"). Today the song of the house finch can be heard from Ontario to Hawaii and from Florida to Oaxaca. House finches have not just colonized these new areas but have thrived, becoming among our most familiar year-round backyard birds. Their total number in North America was recently estimated at more than a billion birds, a significant portion of which live east of the Mississippi.

As they spread across the continent, house finches faced an array of diverse new climates and habitats. Consider the differences in temperature and humidity between California's coastal oak savanna (part of the species' historical range), the Hawaiian Islands (from suburban Honolulu to 6,000 feet up the slopes of Mauna Loa on the big island of Hawaii), southern Michigan, Long Island in New York State, the Rocky Mountains of western Montana, and southern Alabama. These sites range from tropical to cold-temperate, from arid to extremely humid, from high elevation to sea level, from windy to calm, and from having extreme seasonal changes to virtually no seasons at all.

Given the wide range of environments to which the house finch is now exposed, we wondered if the birds that had settled in different areas had become different in physical appearance. We chose seven populations for which we knew the history of colonization, and we measured the size and shape of individual birds. Surprisingly, given the brief time since some of the populations had diverged and had settled in their new environments, we found substantial—up to 10 percent—differences in the size and shape of individuals among populations. Moreover, the patterns of variation were complex. It was not simply that birds in the North were big and birds in the South were small. Within most populations, males and females differ in size and shape, that is, they are sexually dimorphic. We found, however, that male and female house finches were changing seemingly independently, resulting in differing degrees of dimorphism from population to population. In some populations, the males had longer tarsi (lower legs), whereas in others, the females had longer tarsi. The same held for body mass and bill size. And most surprisingly, house finch populations separated for only decades were as different as finch populations that we knew had been separated for hundreds or thousands of years.

Once we had documented that rapid change had occurred in the sizes and shapes of males and females, we wanted to find out what environmental pressures were responsible. Choosing two populations that live and breed at the climatic extremes of the species' range—hot, humid lowlands in Auburn, Alabama, and cold, arid mountains in Missoula, Montana—we monitored thousands of finches (color-banded so that we could distinguish individuals) for six years.

The close match between house finch appearance and environments has come about in a mere fifteen years in some cases.

Our investigation required more than simply catching and measuring birds. We needed to follow individuals all year to gather data on how certain aspects of size and shape correlated with survival, success in attracting mates, and the number of young produced (fecundity). We found that populations differed in which one of these three factors had the greatest impact on the birds' size and shape. In Montana, for example, higher fecundity was most strongly affected by body size, whereas in Alabama it was survival that was strongly impacted by body size.  The reasons for these differences are unknown, but it may be that the Montana population is still expanding rapidly, making fecundity particularly important, while in the warm, wet climate of Alabama, avoiding parasites and diseases may be the key to success (see "Backyard Epidemic"). We also found that the specific size of a trait could be beneficial in one context but not necessarily in another. For instance, in Montana, males with longer wings were more successful in attracting mates. Conversely, smaller males survived better than large males in both populations, but the effect of size on survival was much greater in Alabama.

The key finding from our geographical studies was this: males and females display a size and shape that is the most beneficial for survival and reproduction in their local environments. In a population where females with shorter tails have higher survival and fecundity, females have shorter tails than do females from other populations; in populations where males with deeper bills have higher survival and fecundity, males have deeper bills compared with those of other populations, and so forth. And this close match between the physical appearance of males and females and their environments has come about in a mere fifteen years for some populations.

But we are left with a number of basic questions: What is the mechanism for the remarkable divergence among finch populations? Does the match between birds and their environments represent a genetically based change or simply a plasticity in physical traits that the house finches possess, enabling them to accommodate environmental variation? Especially puzzling is the divergence between the sexes: How do males and females end up looking so very different from each other in different environments when the sexes are virtually genetically identical?

The most straightforward mechanism by which populations of house finches could have achieved such divergence is that, in each population, the finches physically unsuited to the rigors of the new environment were removed from the population by dying or by failing to produce young. The progeny of survivors then inherited beneficial physical traits; the physical appearance of individuals changed over generations; and the population divergence evolved over time. Because we knew the strength of natural selection in our two study populations and the degree of genetic variation in their physical traits, we could calculate the number of generations necessary to accumulate the differences we were seeing. We found that if the population differences indeed represent evolutionary change (that is, genetically based changes in physical traits across generations) in response to distinct selection pressures, then hundreds of years would be needed to produce such divergence. Yet we knew that the populations became established in their environments only in the last few decades, so the adaptive changes must have occurred very recently.

We found that the main limitation for rapid evolutionary change in response to the different environments of Montana and Alabama is that males and females are nearly identical in the genes that code for size and shape. This means that any evolutionary change in size or shape in one sex will be accompanied by an identical change in the other sex. Because the sexes play different roles in reproduction, natural selection often favors different physical appearance in males and females within and among populations. However, the shared genes strongly limit the ability of one sex to evolve local adaptations independently of the other sex, at least over short periods of time. Yet the sexes differ in timing and rate of growth; thus, selection on growth itself can be very effective in accomplishing rapid changes in sexual size dimorphism in adults. So we turned our attention to processes that can alter the way the sexes grow.

The series of changes that occur in an animal as it proceeds from a single fertilized egg to a fully developed adult involves the massive replication and differentiation of cells and tissues. Different parts of the body have to be created and enlarged in precisely the right sequence relative to other parts of the body, or serious problems arise. Minute changes in growth can lead to large changes in adults. At the same time, mistakes in development are typically lethal, so in most birds the rate and timing of growth are not easily modified by the environment.

It seems house finches have somehow circumvented this problem. After measuring the growth of hundreds of nestlings in both populations, we found that each population's timing and rate of growth are highly distinctive and that these growth patterns produce the size and shape best suited to the particular environment of each population. Given that the environments of Montana and Alabama are so distinct, it is not surprising that the growth patterns of the two populations turned out to be different. They were, in fact, opposite. In general, females tended to grow faster in Montana, while males tended to grow faster in Alabama. Correspondingly, in Montana, adult females were larger than males, whereas in Alabama, males were larger than females. The finding that modifications of growth patterns were responsible for the rapid changes in finch morphology between distinct environments left us with another mystery. How had the growth of male and female finches been modified to match their local environments so perfectly?

In Montana, females tend to produce daughters in first-laid eggs and sons in last-laid eggs. In Alabama, the pattern is the opposite.

To find out, we had to start at the first stage of growth: the egg. House finch females lay one egg per day until a clutch, typically five eggs, is complete. Embryos in the eggs do not begin to develop until their mother warms them through incubation. This allows the female to control when the eggs hatch. She can synchronize hatching by waiting until the last egg is laid before she begins the twelve-day incubation, or she can stagger hatching by beginning incubation before the last egg is laid. House finch females typically begin incubating two or three days before the last egg is laid, giving early-laid eggs a developmental head start over later-laid eggs. Because the entire brood of young house finches spends a total of fifteen days in the nest after the hatching of the first egg, this means that compared with last-hatched chicks, chicks from first-laid eggs can get up to five more days' (up to 33 percent more) post-hatch time in the nest, during which they are cared for and fed by parents. Not surprisingly, chicks from the first and the last couple of eggs in a clutch grow very differently and fledge at different sizes.

Amazingly, female finches utilize this simple and predictable relationship between hatching order and chick growth to produce offspring that match the local environment. In Montana, where small males and large females do best, breeding females tend to produce daughters in first-laid eggs and sons in last-laid eggs. Conversely, in Alabama, where large males are favored, the first-laid eggs are usually sons, and the last-laid eggs daughters. Moreover, in both populations, sex and hatching order greatly influence growth rate and size at fledging. For example, in Montana, males from first-laid eggs grow fastest and are larger at fledging than are males that hatch from subsequent eggs, whereas last-laid females grow the fastest and are larger than other females at fledging. The patterns are opposite in Alabama. Because size at fledging often determines the survival of young birds, it seems that breeding females speed up the growth of nestlings that would otherwise be at a disadvantage due to their hatching order.

This strategy has an enormous impact on the eventual size and shape of adults in the population. By "designing" young to fit the environment by modifying their growth and sex in relation to their egg-laying order, mothers improve the chances that offspring will survive. By our estimates, 10 to 20 percent more offspring survive to adulthood than would survive if male-female hatching order were random. This could make the difference between house finches successfully colonizing a region or going extinct when faced with a novel environment, and it may be a primary reason that house finches have been able to spread into an array of environments over such a short time.

Size affects survival, and females seem to speed up the growth of nestlings that would be at a disadvantage due to their hatching order.

Our next step with the Alabama and Montana finches was to devise an experiment to help answer the latest set of questions that arose. Just how does place in the laying order determine growth rate and final body size? Does something in the eggs themselves produce the difference, or is the critical factor sibling competition or differences in the parental care that nestlings receive as they grow? We were able to rule out some explanations with a simple egg-switching experiment in which we exchanged eggs among the nests and modified their original hatching order. For example, we wanted to know what would happen if we took a fifth-laid egg from one nest and put it into the second-laid-egg's place in a foster nest. By switching eggs and then observing the growth of the exchanged nestlings, we found that the original laying order influenced the growth and final size of nestlings much more than the hatching order in the foster nest. That is, the nestling from a fifth-laid egg grew up to look like a fifth nestling even when it hatched in the second position in a foster nest. So, whatever makes early- and late-laid eggs grow differently is already present when the egg is laid. Interestingly, we recently found that females modify the size of eggs in relation to both the gender of an embryo and the laying order, so that the more rapidly growing nestlings hatch from the larger eggs.

Thus, we discovered what may be one of the main mechanisms underlying both the rapid divergence in physical traits among populations and the successful colonization of novel environments by house finches. As tends to be the case in scientific investigations of complex phenomena, however, we have simply replaced one set of questions with another, perhaps more challenging, set. It remains unknown how females modify the sex and growth of nestlings and especially how they make modifications so their young are well suited to the local environment. The resolution of how females achieve these feats will be the focus of future studies, and it promises to keep us busy with this common yet amazing songbird for years to come.

 
Hollywood, Honolulu, and Hoboken

Throughout the nineteenth and into the early twentieth century, house finches were popular cage birds in the United States (as they still are in parts of Mexico). The birds were shipped, probably as pets, to Hawaii in the mid-nineteenth century, and some of these translocated finches established wild breeding populations that soon spread to all the major Hawaiian Islands. Many house finches were also imported to East Coast cities, including Boston and New York, where they were marketed as "Hollywood" finches. After the Migratory Bird Treaty Act was signed into law in 1918, the shipment of house finches as pets became illegal, but the trade apparently continued unabated for decades. In the summer of 1939, however, law enforcement agents began to crack down on the illegal sale of Hollywood finches in New York City. To avoid fines, some pet store owners simply released their stock of house finches onto the streets of the city. Contrary to expectations, many of the released birds survived. Through the 1940s and 1950s, a small breeding population hung on in the immediate vicinity of New York City. By the early 1960s, the eastern population had begun to grow and spread, and by the late 1980s, house finches had settled in across the eastern United States and southern Canada.—A.V.B.



 
Backyard Epidemic

Birds colonizing a new area are exposed not only to different temperatures, humidity, and food availability but also to new sets of pathogens. After getting a foothold in the vicinity of New York City, the eastern population of house finches began to grow at an exponential rate. In 1994, in the midst of the finches' explosive population growth and expansion, an observant birdwatcher in Maryland noticed that some house finches at his bird feeder had grossly swollen eyes. When some of these sick birds died in his yard, he sent the remains to experts on avian pathology, who determined that the finches were infected with the bacterium Mycoplasma gallisepticum. This pathogen, which causes a well-known poultry disease, had never before been found in songbirds. Apparently, house finches feeding around poultry barns in Maryland had contracted a mutant strain of M. gallisepticum that was able to survive and reproduce in their bodies and that led to upper respiratory and eye infections. The pathogen spread through moisture droplets. Bird feeders, so common in the East, became transmission centers as infected birds left droplets that were then picked up by other house finches.

From 1994 to 1996, epidemics of M. gallisepticum spread north, west, and south from the Maryland point of origin. More than 100 million birds—half the house finches in eastern North America—perished. The eastern house finch population is no longer growing but appears to be stable. Moreover, it is showing signs of developing some resistance to the disease. If exposed to the pathogen, the finches in the western population would be highly vulnerable. At present, only the scarcity of finches in the Great Plains has prevented transmission of the disease to the West.—A.V.B.


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