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Santiago y Catherine Escuain
Apartado 13
E-17455 Caldes de Malavella
(Girona) ESPAŃA
escuain@eresmas.net
Website: http://www.sedin.org/
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Avian Quick-Change Artists
Exemplars of rapid adaptation, house finches show that mothers know best.

By Alexander V. Badyaev and Geoffrey E. Hill

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.

Oryginal:
http://www.amnh.org/naturalhistory/0602/0602_feature.html

Patrz tez ogólnie "Natural History":
http://www.amnh.org/naturalhistory/index.html

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