Behavioral Ecology Vol. 12 No. 4: 511-512
© 2001 International Society for Behavioral Ecology
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Flight, fitness, and sexual selection
Laboratoire d'Ecologie Evolutive Parasitaire, CNRS FRE 2365, Université Pierre et Marie Curie, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France, and Museo Nacional de Ciencias Naturales (CSIC), Dept. Ecología Evolutiva, J. Gutierrez Abascal 2, E-28006 Madrid, Spain
Address correspondence to A.P. Møller. E-mail: amoller{at}hall.snv.jussieu.fr .
Received 5 June 2000; revised 27 September 2000; accepted 27 September 2000.
Buchanan and Evans (2000
)
have recently suggested that the length of the tail streamer of the barn
swallow Hirundo rustica is influenced to a large extent by natural
selection, although sexual selection also plays a role. This conclusion was
reached from analyses of video films of the flight of males and females after
reducing the length of their tails by a variable amount ranging from 0 to 20
mm. Evans (1998) has previously
made a similar experiment with a 20 mm manipulation. The optimum phenotype was
subsequently derived from analyses of the flight parameters, while taking a
number of other factors such as sex, farm, morphology, and date into account.
Here we suggest that although it is likely that in fact streamer evolution was
due to both natural and sexual selection, there is little direct evidence to
support the reported conclusions. Although natural selection obviously plays a
role in determining the selective landscape affecting tail length (e.g.,
Møller, 1989;
Møller et al., 1995;
Saino and Møller, 1996;
Saino et al., 1997), it is far
from clear that the cost is mainly measured in terms of foraging ability.
Other factors like parasitism and disease have already been shown to be
important (Saino and Møller,
1996; Saino et al.,
1997). The reasons why the paper by Buchanan and Evans
(2000) does not resolve whether
tail length is mainly influenced by natural or sexual selection are as
follows. (1) Buchanan and Evans did not standardize the conditions under which
the measurements were made. (2) They provide no direct evidence for any of
their aerodynamic parameters having a fitness consequence. (3) The birds were
filmed at variable intervals since the experimental manipulation. (4) The
context in which the flight behavior was recorded does not represent the
relevant selective pressure.
The first problem concerns lack of standardization of experimental
conditions. Buchanan and Evans
(2000) filmed 68 barn swallows
during brood provisioning of first and second broods. This was done when the
birds were entering and leaving the building housing the nest site. This
procedure (and that adopted by Evans,
1998) is problematic for at
least three reasons. First, the flight trajectory will obviously depend on the
way in which a bird will enter its nest site. Sites differ in location from
those positioned in a way so the bird must turn sharply to enter, to those
that allow a direct, straight approach. Entrances to buildings also differ
from open doors to tiny holes in window, requiring different behavior during
approach. These differences in the nest sites will obviously affect the flight
parameters recorded during the approach. The second reason why the video
recordings are problematic is that the age of the nestlings and brood size was
not standardized (or even entered as covariates in the analyses). Both the
number and the size of the nestlings will affect the work level of the parent
and hence its behavior. We know from extensive studies of barn swallows in
seven European countries that reproductive success increases strongly with
male tail length, but not or only very little with female tail length
(Møller, 1994). Thus,
individuals with different tail lengths will differ in their provisioning rate
and hence working rate. This is likely to have consequences for their flight
performance. Third, there are no fitness consequences of the flight behavior
of parent barn swallows when they approach and leave their nest. A
superficially simple interpretation of the data would be that all these
factors would increase the error term in the analyses, and that the analyses
hence would be conservative. However, interpretations should be made
cautiously when relatively small sample sizes are used. How can we in such
situations discern effects due to experimental noise and true biological
effects? This interpretation is supported by a lack of consistency in measures
between studies. Evans (1998)
reported an increase of flight velocity of 10 m/s, when comparing controls and
birds with 20 mm shortening. Buchanan and Evans
(2000) reported a reduction.
Agility increased from 300 to 600 degrees/s in Evans
(1998), when comparing controls
and birds with 20 mm shortening, while Buchanan and Evans
(2000) report an increase from
2500 to 3000 degrees/s for the same treatments. This lack of consistency
across studies needs explanation, since it is not only caused by differences
in base vs. tip manipulations (see Evans,
1998 where both types of manipulations were done), and it renders
the reported results unlikely to be robust. Alternatively, there are errors in
the calculations and the reported findings. Hence, any interpretation will
depend on whether Evans (1998)
or Buchanan and Evans (2000) is
used as the basis.
The second major problem with the study by Buchanan and Evans
(2000) is that they never
quantify the fitness consequences of the aerodynamic parameters. If there is a
natural selection advantage of long tails in the barn swallow
(Norberg, 1994), it should be
possible to predict reproductive performance, for example measured in terms of
number of fledglings, number of broods and quality of offspring, from the
aerodynamic parameters, as obtained in this experiment. If there is a natural
selection cost of long tails, it should result in a reduction in fitness
components. We have in a large number of studies shown intermediate to strong
effects (explaining 10 to 25% of the variance
[Cohen, 1988] or even more) of
male tail length on reproductive success due to sexual selection (reviews in
Møller, 1994 and
Møller et al., 1998;
more recent studies showing similar effects include
Møller et al., 1998;
Kose and Møller, 1999;
Kose et al., 1999; and several
as yet unpublished studies). This has been done using sample sizes of the same
order of magnitude as those used by Buchanan and Evans
(2000). However, we have been
unable to demonstrate similar effects on fitness components of the females
(Cuervo et al.,
1996a,b),
which contrasts with the large degree of similarity between the sexes reported
by Buchanan and Evans (2000).
Furthermore, we have been unable to demonstrate natural selection advantages
of a long tail in male barn swallows. Suggestions that males benefit from a
long tail streamer (Norberg,
1994) should be supported by rejection of the null hypothesis.
Until that has happened we must as good scientists assume no effects. Most
recently, Cadée (2000) has used natural
variation in tail asymmetry of barn swallows to investigate the consequences
for reproductive success and offspring quality. The latter was measured as
tarsus length, body mass, body condition, the size of the buffy coat (a
measure of health status) and a T cell mediated response to an immune
challenge. None of these variables were related to differences in parental
tail length. This was even the case when examining the quality of offspring
produced by adults with broken, and hence highly asymmetric, tail feathers.
Thus, we can conclude that while sexual selection as measured in different
experiments accounts for intermediate to large amounts of variance in success,
there is not even a small (explaining 1% of the variance [sensu
Cohen, 1988]) effect of natural
selection in this case. Thus, current estimates of natural and sexual
selection pressures on the length of the tail in male barn swallows indicate
that there is at least a difference of an order of magnitude between these two
components. Some might state that it is obvious that aerodynamic parameters as
determined by morphology affects fitness, even when no explicit effects on
reproductive success were found. However, the nest approach flight
investigated by Buchanan and Evans to study the importance of natural
selection on streamer morphology is unlikely to affect fitness components, as
discussed below. Moreover, given that even tiny costs are sufficient to cause
large degrees of evolutionary change, small costs may be sufficient to have
molded the shape of tail feathers during evolutionary time.
Third, Buchanan and Evans
(2000) filmed manipulated barn
swallows from 1 to 7 days after manipulation of the tail feathers. Barn
swallows with manipulated tail feathers have altered flight behavior after
release (own observations), but we would expect that birds eventually adjust
their flight behavior to their morphology. Such adjustment would be adaptive
in the case of feather breakage, which is a common phenomenon in barn swallows
during and after the breeding season (Kose
and Møller, 1999;
Møller, 1994).
Adjustment would also be able to account for the apparent absence of effects
of tail manipulation of females on their fitness components (Cuervo et al.,
1996a,b).
Without entering the interval since manipulation as a covariate in the
statistical analyses, the findings can have been seriously biased by
differences in the duration of habituation to the novel morphology.
The interpretation of the results in terms of costs and benefits and their
evolutionary implications are not straightforward. An example of this problem
can be seen in Figure 3 in Buchanan and Evans
(2000). According to this
figure the experimental change in tail length by 10 mm (the consistent turning
point of Buchanan and Evans,
2000) has to be explained by different mechanisms in long-tailed
and short-tailed birds, while a further reduction reverses the pattern. In
addition, tails that are approximately 100 mm long cannot be explained by any
of the proposed mechanisms, as there is almost no effect of manipulation. A
likely explanation is that it might be difficult to determine costs and
benefits of a certain morphology, if estimates derive from approach flights to
the nest rather than more important foraging flight.
Finally, but not least important, is the time when the birds were filmed. Filming the bird when entering or leaving the breeding site introduces a bias since the flight requirements are different in these two circumstances. Most importantly, the selective pressure associated with flight used when provisioning nestlings is biologically and aerodynamically irrelevant in comparison with foraging flight. This makes it unlikely that the reported results have the evolutionary implications intended. Thus, the authors cannot conclude anything about the evolutionary mechanisms for their experiment, since the relevant selection pressures will operate during foraging (which takes place throughout the year) rather than the actual approach to the nest (which occupies a small amount of the annual cycle).
In conclusion, Buchanan and Evans
(2000) have used potentially
biased data on aerodynamics to test their hypothesis. They have not corrected
their findings for habituation by the experimental birds, and, most seriously,
they have shown no evidence of a natural selection advantage of the flight
parameters caused by experimental or natural differences in tail length. This
suggests that there is no measurable natural selection in their experiment and
hence no measurable fitness consequences of the so-called Norberg effect
(Norberg, 1994).
ACKNOWLEDGEMENTS
A.P.M. was supported by an ATIPE BLANCHE from the Centre National de la Recherche Scientifique. A.B. was supported by DGES with the grant PB 98-0506.
REFERENCES
Buchanan KL, Evans MR, 2000. The effect of tail
streamer length on aerodynamic performance in the barn swallow. Behav
Ecol 11:
228-238.
Cadée N, 2001. Parent barn swallow fluctuating asymmetry and offspring quality. J Avian Biol 31: 495-503.
Cohen J, 1988. Statistical power analysis for the behavioural sciences, 3rd ed. Hillsdale: Erlbaum.
Cuervo JJ, de Lope F, Møller AP, Moreno J, 1996a. The energetic cost of tail streamers in the barn swallow (Hirundo rustica). Oecologia 108: 252-258.[Web of Science]
Cuervo JJ, Møller AP, de Lope F, 1996b. The
function of long tails in female barn swallows (Hirundo rustica): an
experimental study. Behav Ecol 7:
132-136.
Evans MR, 1998. Selection on swallow tail streamers. Nature 394: 233-234.
Kose M, Mänd R, Møller AP, 1999. Sexual selection for white tail spots in the barn swallow in relation to habitat choice by feather lice. Anim Behav 58: 1201-1205.[Web of Science][Medline]
Kose M, Møller AP, 1999. Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the barn swallow. Behav Ecol Sociobiol 45: 430-436.[Web of Science]
Møller AP, 1989 Viability costs of male tail ornaments in a swallow. Nature 339: 132-135.
Møller AP, 1994 Sexual selection and the barn swallow. Oxford: Oxford University Press.
Møller AP, de Lope F, López Caballero JM, 1995. Foraging costs of a tail ornament in the barn swallow Hirundo rustica. Experimental evidence from two populations with different degrees of sexual size dimorphism. Behav Ecol Sociobiol 37: 289-295.[Web of Science]
Møller AP, Saino N, Taramino G, Galeotti P, Ferrario S, 1998. Paternity and multiple signaling: effects of a secondary sexual character and song on paternity in the barn swallow. Am Nat 151: 236-242.[Web of Science][Medline]
Norberg R
, 1994.
Swallow tail streamer is a mechanical device for self-deflection of tail
leading edge, enhancing aerodynamic efficiency and flight manoeuvrability.
Proc R Soc Lond B 257:
227-333.
Saino N, Bolzern AM, Møller AP, 1997.
Immunocompetence, ornamentation and viability of male barn swallows
(Hirundo rustica). Proc Natl Acad Sci USA
94: 549-552.
Saino N, Møller AP, 1996. Sexual ornamentation
and immunocompetence in the barn swallow. Behav Ecol
7: 227-232.
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  K. L. Buchanan and M. R. Evans Flight, fitness, and sexual selection: a response Behav. Ecol., July 1, 2001; 12(4): 513 - 515. [Full Text] [PDF]
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