Behavioral Ecology Vol. 11 No. 5: 515-519
© 2000 International Society for Behavioral Ecology
Evolutionary changes in color patches of blackbirds are associated with marsh nesting
Bell Museum of Natural History and Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108, USA
Address correspondence to K. P. Johnson at the Illinois Natural History Survey, 607 East Peabody Drive, Champaign, IL 61820, USA. E-mail: kjohnson{at}inhs.uiuc.edu .
Received 19 January 1999; revised 20 October 1999; accepted 28 January 2000.
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ABSTRACT |
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Fully unraveling the mechanisms of sexual selection requires an understanding of the variation in secondary sexual traits across species in a monophyletic assemblage and an understanding of the evolutionary relationships between those species. The role of red and yellow male plumage coloration in territory defense and sexual selection has been well studied in the red-winged blackbird (Agelaius phoeniceus), and males of many other close relatives of this species also have what appear to be carotenoid-pigmented patches in their plumage. We explored variation in male plumage coloration across species of New World blackbirds (family Icteridae): traits known to be involved in sexual selection in this group. We document that blackbird lineages in which extant species breed in marshes tend to have evolved from an all-black ancestral plumage to one exhibiting carotenoid plumage patches. The two most likely hypotheses to explain this pattern are (1) increased sexual selection intensity in marshes because of increased variance in territory quality and (2) increased frequency of male-male territorial interactions because of an increased density of territories in marshes, but other hypotheses cannot be ruled out. This pattern is consistent with either intersexual or intrasexual selection and warrants further investigation.
Key words: Agelaius phoeniceus, Icteridae, plumage coloration, red-winged blackbirds, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The presence of elaborate, seemingly costly ornaments in animals has been a puzzle to biologists since the introduction of evolutionary theory. Darwin (1871
) suggested that these
traits could arise due to competition between males (intrasexual selection),
female choice (intersexual selection), or some combination of the two. Recent
focus on sexual selection resulting from female choice suggests several
reasons females might possess preferences for elaborate male traits
(Andersson, 1994;
Møller, 1994). Females
may be selecting ornamented males because they are of higher quality
(Grafen, 1990;
Iwasa et al., 1991;
Zahavi, 1975). Alternatively,
choice by females may set up linkage and a runaway process in which female
choice and male ornaments are associated genetically
(Fisher, 1930;
Lande, 1981;
Pomiankowski et al., 1991). A
third alternative is that females may possess sensory biases for reasons other
than mate choice, and male traits that take advantage of these biases are
favored by selection (Basolo,
1990; Ryan et al.,
1990). In contrast to female choice, generally less theoretical
and empirical attention has been given to how male ornaments might evolve as a
consequence of male-male competition (but see
Tanaka, 1996).
Not surprisingly, given the uncertainty about the mechanisms and selective
forces that have led to elaborate traits in individual species, we know little
about why similar traits might evolve in different species or why traits
should vary between species. Environmental differences may influence the
usefulness of certain types of traits
(Badyaev and Leaf, 1997;
Endler and
Théry, 1996;
Marchetti, 1993;
Wiley and Richards, 1978).
Presumably changes in the costs (e.g., predation risk,
Endler, 1978;
Endler and Houde, 1995) or the
benefits (e.g., sexual selection intensity;
Johnson, 1997) of elaborate
male traits could influence their evolution. Although a few studies have tried
to associate interspecific variation in male traits with changes in
environmental or social factors (Hamilton
and Zuk, 1982; Johnson,
1997; Marchetti,
1993; Read and Weary,
1992), the general importance of environmental factors in shaping
the outcome of sexual selection is unclear. Here we present an analysis of the
evolution of male plumage coloration in a group of blackbirds as it relates to
breeding habitat.
The behavioral and ecological traits of many members of New World
blackbirds (family Icteridae) have been intensively studied (Orians,
1980,
1985; e.g., red-winged
blackbirds, Agelaius phoeniceus:
Beletsky, 1996;
Searcy and Yasukawa, 1995). In
addition, molecular evidence on the phylogenetic relationships among these
species has been obtained (Johnson and
Lanyon, 1999; Lanyon and
Omland, 1999). In this study, we focused on a group of birds
within the family Icteridae termed the grackles and allies. Johnson and Lanyon
(1999) developed a molecular
phylogeny for this group based on approximately 2000 base pairs of
mitochondrial DNA sequences. Previous comparative study in the grackles and
allies (Searcy et al., 1999)
has indicated that polygyny in Agelaius-type blackbirds evolved in
the context of marsh nesting, suggesting that habitat may play an important
role in the evolution of behavioral traits. Verner and Willson
(1966) suggested that habitat
may influence the evolution of breeding system in such a way under their
polygyny threshold model.
We extended the comparative study of behavioral traits by Searcy et al.
(1999) to examine the
evolution of sexually selected morphological traits in the grackles and
allies. The plumage of males within this group varies from nearly all black or
glossy in coloration to a black background with yellow, orange, or red patches
of coloration (presumably carotenoids). Often this coloration is confined to a
small patch on the wing (wrist), termed an "epaulet" (e.g.,
red-winged blackbird). Epaulets in red-winged blackbirds are
"coverable" and are often generally hidden when a male is not
displaying or not in an agonistic encounter. It is not known whether epaulets
are coverable in all blackbird species which possess them. In the red-winged
blackbird, this epaulet is vital to intermale territorial defense, and
experimental removal of the epaulet causes males to lose their territories
(Peek, 1972;
Smith, 1972), which are
important components of mate attraction
(Picman, 1981). Because it
appears that sexual selection may be an important factor promoting the
maintenance of epaulets, we wanted to determine what factors were associated
with their origin. We tested for the importance of habitat on signal evolution
(Marchetti, 1993). In
particular, because species of blackbirds appear to have independently evolved
the marsh nesting habit (Johnson and
Lanyon, 1999), we wanted to determine if this change in habitat
influences the evolution of coloration and/or epaulets.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We scored each species within the grackles and allies (as defined by Johnson and Lanyon, 1999
) for
the presence of marsh-nesting habit, the presence of plumage patches of
carotenoid pigmentation (yellow, orange, or red) on the surface of the
plumage, and for the presence of an epaulet (a yellow, orange, or red patch on
the wrist, sometimes termed the "shoulder"). Although there is no
direct evidence that these colors are carotenoid based in all blackbirds, most
red and yellow coloration in the plumage of birds is thought to be carotenoid
based (Gray, 1996) with a few
notable exceptions (hummingbirds, parrots, turacos). We scored species for
male carotenoid patches and epaulets using plates in various identification
guides (Bond, 1993;
Howell and Webb, 1995;
Jarmillo and Burke, 1999;
Ridgely and Tudor, 1989), and
we scored marsh nesting using the definition and states in Orians
(1985) and Jarmillo and Burke
(1999). We also obtained an
independent scoring of male plumage to verify our scoring. We reconstructed
evolutionary changes using MacClade
(Maddison and Maddison, 1992)
with unordered parsimony over the rooted ingroup phylogeny for the grackles
and allies.
Using the reconstructions, we tested for an association between changes in
plumage coloration (gains and losses of carotenoid patches or epaulets) with
breeding habitat using the concentrated changes test
(Maddison, 1990). That is, we
tested the hypothesis that gains in plumage coloration are concentrated on
branches that have marsh nesting as the reconstructed state. In cases where
more than one most parsimonious reconstruction was possible, we conducted the
concentrated changes test with both ACCTRAN (favors reversal over independent
gains of character states) and DELTRAN (favors independent gains over
reversals) reconstructions.
The concentrated changes test lacks statistical power when the number of
evolutionary changes is low (Maddison,
1990). Thus, as an alternative approach to examining the
correlation between plumage coloration and nesting habitat, we used the
maximum likelihood methods of Pagel
(1994,
1997) to test for an
association between discrete character state changes. We fit a model of
independence between characters and compared the likelihood of this model to a
model with parameters for character dependence using likelihood ratio tests.
We used the computer package DISCRETE (available from M. Pagel) to perform
these analyses, and all parameters were unrestricted. Because this analysis
relies on heuristic methods that can vary from run to run, we performed each
analysis five times to determine the stability of the results.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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For both carotenoid plumage patches and epaulets, only one reconstruction is obtained (Figures 1 and 2). Carotenoid plumage coloration is gained five times independently, and an epaulet is gained four times independently. Neither character shows losses. Both reconstructions indicate that an all-black male is the ancestral condition for the grackles and allies clade. Thus, the gains of carotenoid coloration (or epaulet) become the evolutionary events of interest. Four reconstructions of marsh nesting are possible (Figure 3). All four agree in reconstructing the ancestor of the grackles and allies as nesting outside a marsh.
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The concentrated changes test
(Maddison, 1990) indicated
that the gains in carotenoid plumage coloration are significantly associated
with marsh-nesting habitat (ACCTRAN, p =.002; DELTRAN, p
=.031). The significance of the association between gains in epaulets and
marsh nesting depends on reconstruction method for marsh nesting (ACCTRAN,
p =.01; DELTRAN, p =.098), but in either case a positive
association is indicated.
Comparisons of maximum likelihood models for character dependence with
those of independence for carotenoid pigmentation and marsh nesting produced
likelihood ratio statistics ranging from 16.4 to 38.2. The model of character
independence for carotenoid plumage coloration and marsh nesting can be
rejected at p <.01 in all cases. Similarly, comparisons of
independent and dependent models for epaulets produced likelihood ratio
statistics ranging from 11.5 to 31.7 (p <.05 in all cases). Thus,
there is also a significant correlation between epaulets and marsh nesting
using the maximum likelihood methods of Pagel
(1994,
1997).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Both the evolution of carotenoid plumage coloration and epaulets are associated with marsh-nesting habitat in the grackles and allies group of blackbirds. This association is robust to reconstruction method for carotenoid plumage coloration. However, the significance of the association with gains in epaulets is mildly sensitive to reconstruction method for marsh nesting. The power of the concentrated changes test is sensitive to the number of changes in the dependent character (Maddison, 1990
), and in this case epaulet shows fewer changes than
carotenoid pigmentation, so detecting a significant association with marsh
nesting will be more difficult. However, a maximum likelihood method to test
for character association (Pagel
1994,
1997) also revealed a
significant correlation between coloration or epaulets and marsh nesting, so
we consider these results robust to method of analysis.
Although it appears clear that nesting in marsh habitat favors the
evolution of carotenoid plumage patches as opposed to an all-black plumage in
male blackbirds, there are several possible explanations for this pattern,
including direct female choice on plumage, higher intensity of sexual
selection in marshes, a higher frequency of territorial interactions in
marshes, the nature of carotenoid signals, and the signaling environment of
marshes. First, it could be that male plumage pattern is the result of direct
female choice for carotenoid color (intersexual selection). In the
marsh-nesting red-winged blackbird, however, there is little evidence that
females select any aspect of males when making a decision to settle on a
territory (Beletsky and Orians,
1996; Picman,
1981); aspects of the territory seem to be more important
(Picman, 1981). Although
plumage could play a role in extrapair copulations, neither the size nor color
of the epaulet in red-winged blackbirds correlates with male reproductive
success measured by extrapair paternity
(Weatherhead and Boag, 1995).
Thus, it seems unlikely that variation between species in direct female
preferences for plumage coloration could be responsible for the association
between carotenoid color patches and marsh nesting.
Another possibility is that marshes vary greatly in territory quality
compared to other habitats. If this were the case, there would be more
opportunity for females to assess and choose on the basis of territory
quality, resulting in a higher intensity of sexual selection in marshes. In
this case, sexual selection results both from female choice for territory
quality and from male-male interactions in defense of those territories.
Unlike many passerine birds, red-winged blackbirds have a high frequency of
polygyny, suggesting a high sexual selection gradient
(Beletsky, 1996), and polygyny
in Agelaius-type blackbirds seems to evolve in the context of marsh
nesting (Searcy et al., 1999).
Most data seem to indicate that harem size (the number of females nesting in a
male's territory) is larger in marshes than in upland habitats for red-winged
blackbirds (Beletsky, 1996). In
addition, harem sizes in marsh habitats seem to be quite variable, and it may
be that there is more variance in harem size in marshes compared to other
habitats. Further examination of this possibility is needed to completely test
for increased sexual selection intensity in marshes. Comparisons of the
variance in male reproductive success in different habitats would provide a
further estimate of differences in sexual selection intensity.
A third possible explanation for bright coloration in marsh-nesting
blackbirds is that increased male-male competition in marshes requires
colorful signals. For example, a higher density of males in marsh habitats
could increase the number of agonistic interactions, selecting for signals
that are useful in territory defense. Marsh habitats are known to be more
productive than most other habitats in terms of food availability
(Orians, 1980). In addition,
the density of nesting territories in marsh-nesting blackbird species is much
higher than the density of territories in species that do not nest in marshes
(Orians, 1980). If the
frequency of territorial encounters depends on density, then territorial
encounters should be much higher in marshes. Searcy and Yasukawa
(1995) compared intrusion
rates for red-winged blackbirds in marshes with those in upland habitats. Some
studies suggest that trespass rates on male territories are indeed higher in
marshes, but other data appear to be equivocal on this issue. If trespass
rates are higher in marshes, then males in marshes should have more intensive
signals that are used in territory defense. It is well documented that the red
epaulet in the red-winged blackbird is essential in obtaining and defending a
territory (Peek, 1972;
Smith, 1972); thus, it seems
likely that increased territorial encounters is a possible explanation for the
evolution of carotenoid patches and epaulets upon the invasion of marsh
habitats. Comparisons of territory density and the frequency of agonistic
interactions across species of blackbirds would aid in further testing of this
hypothesis.
A fourth possibility is that marsh habitats favor carotenoids as signals
per se, rather than some other form of visual signaling. Although we have no
direct evidence that the red, yellow, and orange colors in blackbirds are
carotenoids in all species, this is likely the case given the distribution of
these pigments in other birds (Gray,
1996). Carotenoids can have immune-system-enhancing properties.
(Olson and Owens, 1998). If
there are more parasites in marshes (e.g., vectored by mosquitoes), then an
enhancement of the immune response may be selected for, and carotenoid plumage
may be a coincident signal. Alternatively, carotenoids also have antioxidant
properties (Olson and Owens,
1998) and may reduce the effects of free radicals in times of
intense competition. If male-male competition is more intense in marshes (see
above), the carotenoids in plumage may signal a male's ability to withstand
the detrimental effects of competition for territories. Both of these
possibilities require more information regarding the role of carotenoids in
the physiology of blackbirds.
Finally, perhaps environmental characteristics of living in marshes favor
the use of certain types of signals. For example, some lekking species of
birds in tropical forests use plumage color combinations that most take
advantage of the ambient spectrum of light. In addition, the timing of
displays and placement of leks are such that these take advantage of optimal
ambient light conditions in the forest
(Endler and
Théry, 1996). Perhaps the open
nature of marshes favors a visual signal (a bright contrasting plumage patch)
compared to other habitats. If the sight distance is higher in marshes, then
visual signals would be more effective. In addition, given longer sight
distances, selection may favor a visual signal that is coverable. If epaulets
are coverable in all marsh blackbirds, this may explain the additional
correlation between epaulets and marsh nesting. However, in
Phylloscopus warblers, species that live in dark habitats have
brighter plumage patches (Marchetti,
1993), opposite the pattern in blackbirds. We also note that many
all-black species of blackbirds nest in open habitats that are not marshes
(e.g., Brewer's blackbird in savannas;
Orians, 1985). Thus, it seems
unlikely that openness of habitat per se is a major factor driving the
evolution of plumage patches in marsh-nesting blackbirds. However, further
comparisons of visibility and the ambient light spectrum across habitats are
needed before this hypothesis can be ruled out.
In general, many examples of the independent evolution of carotenoid
plumage coloration in marsh-nesting habitat occur within the grackles and
allies. This fact provides a tremendous opportunity to study factors that
favor the repeated evolution of similar habitat selection, morphological
traits, and behaviors in this group (e.g.,
Searcy et al., 1999). For
example, several members in disparate lineages in this group were all placed
within the genus Agelaius because of this convergence which obscured
evolutionary relationships. To fully study evolutionary patterns in this
group, it will be important to compare many different species in their
habitats, morphology, and behaviors. Although the red-winged blackbird
provides a model system within this group, previous studies on this species
can also be used as a framework for the study of other close relatives, and
these comparative studies would aid in understanding the forces that mold the
evolution of traits.
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ACKNOWLEDGEMENTS |
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D. H. Clayton provided useful discussions during the writing of the manuscript. E. Burtt, Jr., D. Drown, and B. Moyer provided valuable comments on this manuscript. R. J. Adams provided an independent scoring of male plumage. During the writing of the manuscript, K.P.J. was supported by National Science Foundation CAREER award DEB-9703003 to D. H. Clayton. M. Pagel kindly provided the computer package DISCRETE to conduct the maximum likelihood analyses.
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