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The Fitness Consequences of Inbreeding
Sex-biased Dispersal, Kin Avoidance, and Kin Selection
Outbreeding Depression and Female Choice for Natal Song
Extinction, Colonization Success and Dispersal
Bees and Polarized Light
Migration and Navigation in Birds
The Sun Compass of Birds
Stellar Navigation: "I got the sun in the morning and the stars at night"
Planetarium Star Shifts
Learning or Instinct of the Stars?
Dispersal results in a tendency for animals that were once aggregated, to become more widely distributed through movement away from aggregations. The most common aggregrations found in nature are associated with the nest site. Hatching juveniles or fledglings leave from a concentrated place, and attempt to find a site that they might live in for most of the rest of their life. Such long distance movement can be extreme in the case of birds. Rare dispersal records based on banding at the nest and recovery by other ornithologists have registered dispersal distances measured in 1000's of kilometers. Now this is not surprising given the flight capabilities of birds. Dispersal of mammals is measured on the scale of tens of meters and kilometers. Records for lizards place the upper limit on dispersal at 1.5 km. Given the length of a hatchling (2.5 cm), and the distance traveled, 1.5 km * 1000 m/km * 100 cm/m this would amount to 60,000 body lengths or put into human body lengths (2m tall), the human equivalent of 120 km traveled in the first week or two of life.
What could be worth travelling such inordinate distances?
There must at the very least be incredible energetic costs to such long distance movement. In addition, there might be a disadvantage measured in terms of survival. A moving animal may be at great risk of predation. We will explore two theories that might explain why juveniles of most species tend to disperse:
Inbreeding can be defined in many ways, but we generally think in terms of the simplest definition which has to do with matings among related individuals. However, as all humans ultimately share some related individuals (e.g., the proverbial adam and eve) at some point during their remote past, this definition is not all that precise. A more precise definition that also has some practical merit is to express inbreeding as the probability of the two alleles on complementary chromosomes being identical by descent. If these two copies of the allele (one from mother and one from father) are identical by descent, then they must have arisen in the not-so-remote past from a single strand of DNA. Calculations concerning the probability of identity by descent has some practical merit because it can be used to calculate the risk that a a deleterious recessive mutation might show up in an inbred individual. If an individual has two identical copies of a deleterious rececessive mutation, that individual will express a trait that in some way lowers fitness, or in the worst case of a deleterious recessive lethal, will cause death.
The easiest way to get two genes together that are identical by descent is from a consanguinous mating, or a mating among close relatives. Consider progeny fertilized from a mating between a mother and son and try to track the alleles coming from the mother. We will track one allele, bb, from mother to son and from the mating of mother and son which we will call an oedipal mating. (Recall that each pair of chromosomes posseses two sister chromatids). The allele b is located on one of the mother's two chromosome pairs.
The son may receive one copy of allele b with probability of 1/2 and this transmission is denoted by the red line.
The blue lines denote the 1/2 probability that the mother will contribute the b to a progeny sired by her son, who also contributes allele b with probability 1/2 via the second blue line.
Because all events are mutually independent, we multiply all of the probabilities to get the net probability that a child produced by an oedipal mating possesses two bb alleles:
1/2 * 1/2 * 1/2 = 1/8 (eqn 1).
Note that, the "a" copy could just as easily been transmitted to the son in the first place so the total probability that the alleles in the oedipal child are identical by descent can be achieved two ways, either with allele "a" or with allele b and the probability of inbreeding from an oedipal mating is:
2 * 1/2 * 1/2 * 1/2 = 1/4 (eqn 2).
Of course, there is a 3/4 probability that the oedipal child is not identical by descent. Let us consider a few special cases to assess the fitness consequences of such inbreeding. If mom was a carrier for a single deleterious recessive allele, b, then the probability that a son produced from an oedipal mating would die is given by the probability that a single allele is identical by descent = 1/8. (Note that mom has one good copy in the form of allele "a".
If the mom happened to carry an allele that was deleterious on each of two different genetic loci we would multiply this value by 2 to get the probability of a progeny from an oedopil mating getting at least one such double whammy = 2 * 1/8 = 1/4. Because each an individual may possess several deleterious recessive alleles, matings among related individuals typically produces inbreeding depression or a reduction in fitness that arises from identity by descent. Such alleles do not have to be lethal, rather the combination of several mildly deleterious alleles can have a dramatic impact on fitness.
As a second example, let us consider the possibility of a sib-sib mating. We now have to keep track of the fathers alleles because a grandchild can become inbred from one of the mom's alleles or one of the the father's alleles. Again, we will track one allele, bb, from mother to son and from the mother to daughter. At the end we will then multiply the probability of a single allele being identical by descent by four (all possible alleles that might be identical by descent) to determine the overall probability that any allele is identical by descent.
The mother gives the b allele to her son with probability of 1/2 and likewise the daughter receives the b allele with probability of 1/2 (both denoted by the red lines). Given that the daughter received the b allele, the daughter passes the allele on to her own progeny with propbability 1/2 (blue line). Likewise, given that the son has the b allele he passes it on to his progeny with probability of 1/2.
The, probability that the grandchild received two copies of the b allele is given by:
1/2 * 1/2 * 1/2 * 1/2 = 1/16.
Finally, we realize that the grandchild could just as well have received the a, b, c, or d alleles by the same routes with the same probabilities so the probability of any two alleles at a single locus in the same individual being identical by descent is given by:
4 * 1/2 * 1/2 * 1/2 * 1/2 = 1/4.
The same logic can be used to compute the probability of two cousins yielding a child that has genes identical by descent, though the length of the paths are a little bit longer. Indeed, the logic used above can be used to compute the probability of inbreeding or identity by descent for any consanguinous mating. The inbreeding in any set of pedigrees can be computed from similar path diagrams that chart the genealogical relationships among individuals.
The fitness costs arising from such inbreeding mechanisms have lead various authors to propose that patterns of sex-biased dispersal are a kin avoidance mechanism. The tendency for offspring to breed in their natal home range is referred to as philopatry. Because dispersal per se entails costs, both sexes of progeny need not disperse to dramatically lower the probability of inbreeding. If either the female progeny disperses or the male progeny disperses, the risk of inbreeding is lowered dramatically because one of the most pernicious sources of high inbreeding (sib-sib is eliminated, still have to worry about father-daughter). Most mammals have male-biased offspring dispersal, and the female progeny tend to be philopatric. For example, Kay Holekamp has found that female ground squirrels tend to remain near their natal nest and males disperse several hundred meters away.
The tendency for dispersal in one sex cannot be explained in terms of kin avoidence, but ideas of kin selection must be used to explain why female progeny remain. If female's get assistance from their mother or from sisters, then they would be likely to be philopatric.
Kin selection appears to be related to levels of philopatry in other mammals and the dispersing sex is the sex least likely to benefit from kin selection. For example, in cheetahs, if a female cheetah produces two or more sons, those sons are likely to form a kin group and defend a territory cooperatively. The brothers will even participate in cooperative breeding. It takes a few males to adequately defend a territory against other males.
Conversely a solitary male lion usually heads a pride and there is no advantage to being philopatric in lions. Male lions disperse, whereas females remain with the pride. To further avoid inbreeding between a father and his daughters, many male lions disperse and attempt to take over another pride of lions when his daughters begin maturing. This is fairly common in other groups were the possibility of father-daughter matings arises.
Very little evidence is available that directly links inbreeding depression to lack of dispersal in wild populations, but Packer (1979) reported anectodal information on a male baboon that failed to disperse at sexual maturity. He produced low surviving progeny compared to outbred males in the baboon troop.
Information on inbreeding depression per se is available for cases in which researchers have drawn up pedigrees of the sort shown above. An elegant study of such pedigrees for sparrows on Mandarte Island (XXX and Smith, 1987) illustrates real costs to inbreeding. However, in the case of the song sparrows, the effects of reduced survival in inbred individuals were most strongly manifest during periods of environmental stress. Those individuals with a higher inbreeding coefficient (e.g., the product of one or more consanguinous matings based on the pedigree computations) were more likely to die during a famine than individuals with a low inbreeding coefficient.
While consanguinous matings generally result in inbreeding depression, it is does not follow that an animal sould find a mate that has a completely different genetic background. Outbreeding depression is the tendency to show reduced fitness in progeny that are the product of two very different genetic backgrounds. There may be an optimum level of outbreeding. Indeed the optimal dispersal distance may reflect such outbreeding depression. Go too far and you end up in the company of very different genetic mates. Outbreeding depression is thought to arise from epistatic interactions among loci. A minor amount of incompatibility among a suite of genes involved in some sort of enzyme cascade may lower fitness.
Outbreeding depression may give rise to a behavioral block to breeding that is similar to species recognition mechanisms. For example, many birds are only sexually responsive to mates from their own natal areas. The following experiment illustrates that female birds learn songs of appropriate mates in their youth and then choose rather srupulously regarding males that sing the right song.
Baker first used tudor males to teach young birds a song dialect:
Songs similar to the tudor songs were presented to the females and songs from a different area were presented to the females when they reached maturity:
Baker, found that female white-crowned sparrows responded positively to male courtship songs at a higher rate if the song was derived from their home dialect compared to an alien dialect.
The key feature of this study demonstartes that birds learned the song during the nestling phase. In addition, it is possible to fool females into preferring a truly "non-natal" song, or one from a region other than their true source population. By playing them a song that is from a different source population during the critical song learning period. For example, if tudor songs had been from Gothic the females should have preferred Gothic males at maturity and rejected Sand Creek Songs.
Baker, M. C. 1981. Early experience determines song dialect responsiveness of female sparrows. Science 21: 819-821.
The advantages and disadvantages of dispersal strategies are not limited to genetic costs of inbreeding. Consider, a meta-population in which many sub-populations are found loosely connected and each sub-population is relatively small. Moreover, each sub-population has a modest probability of local extinction where all members of the population might be eliminated by some random environmental disaster.
In such a case, selection will favor individuals that disperse from occupied habitats to those parts of the habitat where a local extinction has occurred. Such disperser genotypes do not have any inside information about the location of "open" habitat, but if a lucky disperser happens upon such unoccupied habitat their reproductive rate will be quite high compared to those individuals found in the occupied and crowded habitat. A disperser landing in an occupied area has low success. Theory predicts that the dispersal tendency will be quite common even with a low frequency of local extinctions of a sub-populations.
The Eastern newt, Notophthamalus viridescens appears to be a candidate for an extreme version of this model. The extinction of newts in a pond is a very likely event if the adults are not successful in producing metamorphlings across a string of bad years (Gill 1980). Adults breed in temporary ponds, and the adults return to the same pond year after year. The reproductive success of newts in any one pond is extremely low, and the newts go extinct in ponds quite frequently. This species of newt has evolved a dispersing phase to its life cycle called the "red eft" that wanders around the woods moving great distances over the course of several years. The eft eventually settles in a pond, and if it happens to settle in a "near empty" pond, with at least one mate, the two metamorphosed newts will likely colonize the pond and have high success if they get lucky. The newts appear to be a case in which an obligate dispersal phase has been favored. All offspring turn into an efts and disperse.
Other species of amphibians illustrate that two or more dispersal types may coexist in the same population. In this case, the dispersal tendency is facultative and triggered by density of conspecifics. Semlitch has identified genetic predispositions for two kinds of salamanders:
The type of salamander that does not metamorphose, also does not disperse and is known as a paedomorphic salamander. Because paedomorphic salamanders remain in the water their entire life, they are susceptible to a large-scale drying event, because they have lost the capacity to metamorphose. However, because paedomorphic avoid the costs of dispersal, they grow to a larger size at maturity, and have a competitive advantage over the form that has the typical amphibian metamorphosis and dispersal phase. Even if the paedomorphic form goes extinct and the pond is recolonized by the typical form, new paedomorphic mutants are probably arising all the time. The evolutionary switch or mutation that gives rise to new paedomorphic forms from the typical forms is very simple. All that is entailed is a downregulation in the genes that cause metamorphosis from aquatic larvae to terrestrial adult (Thyroxine production and regulation). The other more typical form possesses fully functional genes and metamorphoses under most conditions. This form is much more likely to colonize the newly extinct ponds. In the long term, it has an advantage over the paedomorphic form because all ponds will eventually dry up and the population goes extinct. As new mutations can always arise and invade it is an excellent example of a system that has no Evolutionary Stable Strategy. Both forms coexist with one periodically outcompeting the other, yet neither is a longterm winner.
Dispersal is typically associated with a once in a lifetime event -- movement to a new habitat. During the dispersal event, it is thought that animals might make a random movement, and then settle once suitable habitat is found. Once the animal has settled in a suitable patch, it must move around its local universe and not get lost.
We will explore how bees and birds use visual cues such as the sun or the starts to orient. We will consider magnetic navigation in birds. Orientation is the use of external cues to move about the environment. Orientation can come about by fixing a position and then using cues to determine the appropriate direction to move in. Navigation involves a little more sophistication in that a map sense (a sense of where you are) in addition to a compass sense (a sense of the appropriate direction in which to move) are a requirement for a complete navigational system. Many studies have demonstrated orientation, but few have demonstrated that animals have a map sense or a sense of where they are.
Migration is distinct from dispersal in that migratory animals typically move from one geographic region to another,without using the intervening habitat. The movements are associated with a particular season, and invariably tied into the reproductive cycle. A key issue underlying migration is how animals navigate the huge distances or orient to natal areas. Underlying most migrations is a sense of time so that the appropriate season for migration is used. Migration is classically associated with birds. However, many other groups undertake long migratory movements:
A pervasive feature in the environment that animals could use for orientation is the sky itself. The sun rises at specific times during the day, and provided that an animal has a sense of time, the relative position of the sun could be used to determine direction. However, cloudy skies limit the use of the sun as a source of orientation information. What remains intact on even the cloudiest of days is polarized light. Light rays entering the atmostphere become scattered. Owing to some fancy physics, this creates polarized light. The sky in the direction of the sun is less strongly polarized than the sun in the other half of the sky which is maximally poloarized -- even on a partly cloudy day. Of course a cloudy day does obscure the polarization quite a bit, but it remains a steady albeit attenuated environmental cue that could be used if organisms could detect polarized light.
Tough to visualize. Well imagine you had eyeballs sensitive to polarized light and you looked at the sun. The light from the sun is coming from all directions and is not all that polarized, so the sun would look dark (solar sky). As you turn your head away from the sun and look 90 degrees away, the polarized light gets brighter and brighter. Exactly 90 degrees away is the brightest for polarized light because a lot of light rays are heading perpendicular to your field of view. As you continue turning your head, further away from the sun, the polarized light gets dimmer and dimmer, until it is dark again when you are looking away from the sun (anti-solar sky). This is because light is again heading in away in all directions compared to when you are looking 90 degrees from the sun when it is coming from the sun perpendicular to your field of view.
The celestial compass of bees was discovered by somewhat indirect means. Bees go out on foraging flights, find food, then fly back to the hive to communicate to the other workers the source of the food.
The bees use a waggle dance to indicate the direction of the nectar source.
The sun provides a very constant reference in the sky for the bees to
direct other workers. The bee ends its circuit around the loop with a waggle,
and the distinctive waggle part of the dance lines up with a vector that
leads directly to the nectar source. The distance from the hive is proportional
to the number of waggles in the dance.
Karl von Frisch decoded the language of bees using some clever manipulations. The tendency for bees to point in the correct direction of the nectar supply can be plotted on a circle. The height of the histogram is proportional to the number of worker bees thatchoose that vector (i.e., typically close to the actual angle of the plant from the sun if they are correct). Few workers are far off the actual angle.
In the diagram to the right, the Average Angle of the Worker Bees dance
indicates that food is located approximately 100 degrees to the right of
the sun. A worker would fly at a bearing of 100 degrees to the sun and come
upon the source of food that the scout bee had found. It appears that the
worker is using the sun a reference. In actuality the bee is using polarized
light as a reference. The omatidia of the bee contain special photoreceptors
that are sensitive to polarized light in ultraviolet wavelengths.
Wehner and Rossel discovered the workings of the bees celestial compass by manipulate the light coming into the hive while the bee did its waggle dance.
They showed that the sun's rays were not necessary by putting up a screen that eliminated the sun's direct rays from entering the hive, while permitting the skys polarized light to reach the hive through an opening in the top of screen.
Worker bees will display the correct direction to nectar even though
the sun is not visible.
If you block out all polarized light using a plexiglass bubble, you eliminate the cue that the bees use too orient themselves. The plexiglass absorbs polarized light in the ultraviolet wavelengths.
A bee that has come back from its scouting knows the correct angle, but
without the sun to guide it, the worker cannot tell which direction it should
end its waggle so as to direct the workers. The data for a number of workers
shows a very random pattern heading off in every direction compared to the
consistent directions shown above.
Finally, one can let in just certain wavelenghts of
polarized light using filters. In such experiments, the researches keep
altering the wavelengths until the hit upon the exact wavelengths that give
the bees the external information it needs to orient their dances correctly.
Many wavelengths of light give a random orientation to the dance pattern.
However, light in very specific uv wavelengths appears to trigger the polarized
light sensitive regions of the omatidia and allows for correct orientation.
The bee is "blind" to such directional information even if the
light is correctly polarized, but in the wrong wavelengths.
Birds use the sun as a simple compass. How do we know that that they use it for orientation? Like the bees, the birds indicate the direction that they wish to fly by a well known phenomenon called the zugenruhe or nighttime restlessness. Zugenruhe refers to the sharp jump in nighttime activity that occurs at the onset of the migratory response. Because birds migrate at night, but are not normally active at night during other times of the year, students of navigation have used birds as a model system for understanding directional orientation.
Another aspect of zugenruhe is that birds orient strongly in the
direction in which they are to migrate. A clever apparatus consisting of
a cone shaped cage with a mesh top (Emlen 1970), and an inkwell at the bottom
has been developed to record the directionality of the zugenruhe.
The birds hop up and down trying to take flight, and end up leaving a complete
record of each hop, as well as the direction of the hopping relative to
Let's consider Starlings that have a normal migration route that is in a SE direction. It is easy to shift the direction of zugenruhe by using mirrors to alter the true direction of the sun at sunset by 90 degrees clockwise or counterclockwise. Starlings in aviaries that see such a frameshifted sun end up leaving tracks that are 90 degree frame shifted in the appropriate direction.
Researchers hypothesize that the birds take a bearing on the sun at sunset
and then use dead reckoning to fix on a correct direction until sunrise
at which point a new bearing can be used. Regardless of the mechanism, it
is clear that the birds use the sun as a Celestial compass much like bees
used polarized light as a Celestial Compass.
If the skies are overcast, then the birds have a random orientation to their zugenruhe movements. This suggest that the sun is necessary to at least get a quick fix on or the birds do not have a directional cue to initiate their dead reckoning during the night.
If birds do not have the sun, what other cues might they use? Some have suggested the weather. Winds are very predicable at certain altitudes and a stiff cross wind might be used to aid the bird during periods of no sun or to further refine orientation at night. During the day, birds undoubtedly use large landmarks like the Mississippi River, and such bodies of water would also be available at night via the reflection of the moon.
A little primer on stellar navigation.
Some birds are real stargazers, and can use the position of the stars to orient.
Most of us have looked up in the night sky and you may have noticed that
the constellations move during the course of the night. This apparent motion
is caused by our own earth's rotation, and polaris happens to be located
directly along the earth's north-south axis. As the earth rotates, polaris
does not move, but the other starts appear to rotate around polaris which
is the handle-tip to the little dipper.
If birds are set up in a planetarium all of the stars
can be projected on the dome like ceiling, and the rotational position of
the stars can be easily manipulated by the machine that projects the stars
on the ceiling. The orientation angle during zugenruhe can be used
during such manipulations of stellar cues to determine what information
birds might be using at night.
First, Sauer simply manipulated the stars images projected on the dome of the planetarium. He rotated the stars by 180 degrees. The star shift is not just a rotation of the stars (which birds could use as a clock, much like we use the sun during the day), but rather, the orientation of polaris and all stars around polaris are flipped into the souther sky. As predicted, he rotated the direction of the Zugenruhe by exactly 180 degrees. Birds use some kind of view of the stars to orient their zugenruhe.
Emlen conducted an experiment on the early experiences of Indigo buntings with a star map. He set up two groups of chicks that were reared under the following conditions:
As predicted, birds without a star chart did not learn the appropriate cues and showed no orientation.
Those birds with a reversed experience of the stars also showed a reversed Zugenruhe relative to the control birds.
Birds learn the star map in their youth and use this information to orient their Zugenruhe, which is a good thing, as the earth wobbles and thus the star map is not constant, but it changes every 13,000 years or so.
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