Behavioral Ecology Vol. 13 No. 1: 1-10
© 2002 International Society for Behavioral Ecology
Phylogeny, specialization, and brood parasite—host coevolution: some possible pitfalls of parsimony
a Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106, USA b Department of Biology, University of California, Riverside, CA 92521, USA c National Zoological Park, Smithsonian Institution, Washington, DC 20008-2598, USA
Address correspondence to S.I. Rothstein. E-mail rothstei{at}lifesci.ucsb.edu . M.A. Patten in now at the Environmental Studies Program, Dartmouth College, Hanover, NH 03755, USA
Received 21 June 2000; revised 29 December 2000; accepted 5 February 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Coevolutionary hypotheses (COEV) predict that parasitic birds become more specialized in host selection over time as more host species evolve defenses. A contrasting model, PHYLO, suggests that brood parasites exhibit a phylogenetic trajectory toward increasing generalization because there is a positive correlation between present-day numbers of host species and the branching order of parasitic cowbird species in a DNA-based phylogeny. However, this apparent phylogenetic pattern does not conflict with COEV, as some have concluded. Assuming allopatric speciation, which is supported by an area cladogram, COEV predicts a correlation between branching order and host number because the potential hosts of the earliest cowbirds to branch off have had the greatest amount of time to evolve defenses. Although PHYLO is more parsimonious than COEV, the difference is trivial, with the latter requiring only one more evolutionary change in the entire cowbird clade to produce the pattern that exists today. Support for COEV over PHYLO comes from brood parasitic cuckoos, which are much more specialized than parasitic cowbirds and represent an older clade, as shown by new DNA data. Cuckoos also have lower interspecific variance in host numbers than do cowbirds, which conflicts with PHYLO. Unlike COEV, which assumes that the number of hosts a parasite uses is related at least as much to present ecological conditions as to phylogenetic history, PHYLO assumes that current host numbers reflect historical character states. However, host number is labile, with as much variation within as between species. Nor are published host numbers reliable measures of parasite host selectivity, as they are due in part to researcher effort and range size. Although the comparative approach can provide insights into evolutionary history, some coevolved features may be too dynamic to retain a phylogenetic signature, and, in the case of parasitic birds, neither PHYLO nor COEV can be invalidated, although the latter is more consistent with available evidence. Strict adherence to parsimony may often be inappropriate when assessing coevolved characters.
Key words: brood parasitism, coevolution, cowbirds, cuckoos, generalist, parsimony, phylogenetic reconstruction, specialist.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
A commonly addressed issue in studies of parasite—host coevolution is the large range in the numbers of host species used by various parasites (Thompson, 1994
). Birds that
are obligate brood parasites and the species that serve as their hosts are
especially interesting in this regard because of the large range in number of
host species, 1 to > 200, used by different parasitic birds. Accordingly,
parasitic birds and their hosts have been the subject of numerous recent
studies dealing with parasite—host coevolution (Davies and Brooke,
1989a,
b; Lotem et al.,
1992,
1995;
Marchetti et al., 1998;
Rothstein, 1990;
Sealy, 1996; Soler and
Møller, 1990,
1996) and have been the
subject of several books (Davies,
2000; Johnsgard,
1997; Ortega,
1998; Rothstein and Robinson,
1998). In this article, we contrast two conflicting hypotheses
dealing with the evolution of host use in parasitic birds. The first
hypothesis is that parasitic birds become more specialized over time by using
fewer host species and the second is that parasitic birds become more
generalized over time.
The hypothesis of increasing specialization was proposed because hosts
often evolve defenses against parasitism, such as rejection of foreign eggs,
in response to reproductive losses incurred by parasitism. Parasites in turn
often evolve counterdefenses, such as mimicry of host eggs. These
counterdefenses must be specific to a single host species or to a group of
hosts with similar features, such as similar egg types. Because genetic
constraints do not allow a single population to simultaneously maintain
numerous alternative character states, such as many different mimetic egg
types, parasitic birds should parasitize a smaller number of host species as
time passes and as more and more potential host species evolve defenses. Thus,
this body of coevolutionary theory (hereafter COEV) predicts that a parasitic
bird will become more specialized the longer it is in contact with a
particular avifauna (Davies and Brooke,
1989a; Lotem and Rothstein,
1995; Rothstein,
1990).
The alternative to COEV is derived from a phylogeny of parasitic cowbirds
(Molothrus spp.) based on DNA sequence data
(Johnson and Lanyon, 1999;
Lanyon, 1992;
Lanyon and Omland, 1999). The
proposed order in which cowbird species branched off from the rest of their
lineage is correlated with current numbers of known host species, ranging from
one in the earliest branching species to > 200 for each of the two most
recently derived ones (Lanyon,
1992). This correlation led to the conclusion
(Alcock, 1993;
Lanyon, 1992;
Thompson, 1994), based on
parsimony, that cowbirds show a phylogenetic trajectory toward generalization
(hereafter PHYLO) and that this trend toward increased generalization
conflicts with COEV.
While we accept the proposed cowbird phylogeny (it is consistent with DNA
sequence data from two different genes), we argue that the relationship
between this phylogeny and host number is not in conflict with COEV. First, we
review COEV and trends in host use that might be seen in a clade of brood
parasitic birds. Next, we show through use of an area cladogram and
consideration of likely speciation processes that the correlation between
branching order and current host numbers in cowbirds is compatible with both
COEV and PHYLO, although the former provides a more cogent explanation.
Although PHYLO is more parsimonious than COEV, we demonstrate that the
difference is trivial, with the latter requiring only one more evolutionary
change in the entire cowbird clade to produce the pattern that exists today.
We also address the assumption according to PHYLO that current host numbers
reflect historical character states and show that host numbers are instead
labile features sometimes showing as much variation within species as between
species. Nor are published host numbers reliable measures of parasite host
selectivity, as they are due in part to researcher effort and range size.
Finally, we present new molecular data on parasitic cuckoos (Cuculinae) that
show that this group is older than the cowbird clade and is more specialized,
a result consistent with COEV but in conflict with PHYLO. A point central to
much of this article is the argument that present numbers of host species are
not reliable guides to the numbers of hosts parasites had in the past (see
also Davies and Brooke, 1998;
Freeman and Zink, 1995) and
cannot reveal whether specialization or generalization is the primitive
condition. Our results agree with Schluter et al.
(1997), who showed that
determinations of ancestral character states via parsimony can have large
degrees of uncertainty, especially for characters that are continuous, such as
host numbers used by parasitic birds, rather than discrete, and that evolve
rapidly (see also Frumhoff and Reeve,
1994).
A review of parasite—host coevolution in birds
COEV predicts that a parasite's selectivity among hosts is a labile trait
that varies inversely with the extent to which potential hosts have effective
defenses against parasitism. The amount of time over which potential hosts
have been exposed to parasitism will be a major determinant of their level of
defenses. Thus, the longer a parasite interacts with a particular array of
potential hosts, the more likely it is to be specialized; in other words, for
any given interaction between a particular parasite and a particular avifauna,
relative generalization is likely to be followed by specialization, regardless
of a parasitic species' position in a phylogeny. The transition from
generalist to specialist could be gradual, or it might occur in one or more
major steps (Rothstein,
1976).
COEV allows for two exceptions to the trend toward increasing
specialization. First, a specialized parasite should become more generalized
if it colonizes a region where potential hosts are largely lacking in
defenses. Second, if the first obligately interspecific parasite in a clade
evolves from an intraspecific parasite
(Hamilton and Orians, 1965;
Payne, 1977;
Rothstein, 1993), it might
initially have a narrow host range but should become more generalized if there
are unparasitized hosts without defenses. Nevertheless, in both of these
cases, the transition from specialist to generalist is likely to be followed
by increasing specialization as more hosts develop defenses.
In addition to time, the likelihood that hosts will have evolved defenses
also depends on the abundance of parasites, which may include all parasitic
species in a region. Parasite abundance is important because it in part
determine rates of parasitism (Hoover and
Brittingham, 1993) and rates parasitism are a major determinant of
the selective value of host defenses
(Davies et al., 1996;
Rothstein, 1975a). Other
species of parasites can be important because host defenses, such as egg
recognition, are not necessarily specific to the parasite(s) that a host
experiences (Rothstein, 1982a,
b). Thus, defenses evolved in
response to one parasite can give hosts protection against other parasitic
species.
Host defenses are not the only determinant of a brood parasite's degree of
specialization. Even in the absence of host defenses, different sympatric
parasitic species may specialize on different host species to minimize
interspecific competition (i.e., two parasites using the same host nest)
(Brooker and Brooker, 1989a;
Friedmann, 1967).
Intraspecific competition for hosts may also be a factor. A parasite that is
relatively uncommon may specialize on a limited set of high-quality hosts
because individual host nests will rarely be parasitized more than once. But
if a parasite is abundant, selection may favor parasitizing a wider range of
host species, even poor quality ones, to avoid competition in multiply
parasitized nests. So regardless of its branching position in a phylogeny,
COEV states that a parasitic species can be a generalist or a specialist
depending on the number of potential hosts that have effective defenses and on
the intensity of interspecific and intraspecific competition for hosts.
Nevertheless, most generalist parasites should become more specialized the
longer they are in contact with a particular avifauna.
A specialized parasite confronted with a community of potential host
species, nearly all of which have well-developed defenses, may eventually
reach a fairly constant level of specialization in which parasitism is
concentrated on a handful of species. However, even this situation may be
dynamic because the particular species parasitized may change over time
(Brooke and Davies, 1987;
Davies and Brooke, 1989a;
Nakamura et al., 1998;
Rothstein, 1990). A parasite
may shift away from a host whose defenses become highly efficient and begin to
use a past host that has lost all or some of its defenses in the absence of
parasitism, although the period over which host defenses are retained in the
absence of parasitism may be considerable
(Bolen et al., 2000;
Hosoi and Rothstein, 2000;
Rothstein, 2001). Thus, over
time, a specialized parasite may cycle through a large number of host species,
even though only one or a few are used at any one time
(Marchetti, 1992). In sum
then, COEV assumes that the curent number of hosts a parasite uses is related
at least as much to the ecological circumstances it faces as to its
phylogenetic history, whereas PHYLO gives priority to phylogenetic
history.
In this article, we provide four major results: (1) an area cladogram that
considers speciation mechanisms and shows that COEV predicts the present-day
relation between branching order and cowbird host numbers; (2) an analysis
that shows that COEV and PHYLO differ only slightly in terms of parsimony; (3)
data showing that published lists of hosts are subject to biases that
necessitate caution when used to assess evolutionary hypotheses; and (4);
tests that use cowbird and cuckoo data to distinguish between COEV and PHYLO.
These latter tests are based on the pattern that prompted formulation of PHYLO
(i.e., host number increases with time and/or cladogenic events). Thus,
species in older and/or more speciose clades of parasites should use more host
species than parasites in younger, less speciose clades. Similarly, because
PHYLO assumes that specialization is the primitive state, that host number
retains a significant phylogenetic signature, and that host number increases
with time and/or speciation events, it predicts that older clades of parasites
show greater interspecific variation in host numbers than younger clades. COEV
predicts that members of older parasitic clades use fewer host species, but
makes no clear prediction regarding interspecific variation in host numbers
because it assumes that many factors affect host number. We test these
predictions using published DNA data on cowbirds and new DNA data on parasitic
cuckoos to assess the relative ages and host numbers of these two clades. More
specifically, we predicted that parasitic cowbirds are a younger clade than
parasitic cuckoos because the cowbirds comprise 5 similar species in a single
genus whereas the parasitic cuckoos include about 50 species and 12 genera
with a remarkable range of colors, sizes, and forms
(Johnsgard, 1997;
Wyllie, 1981). Given our
prediction about the ages of these clades, which was confirmed, cuckoos should
have more host species and greater variance in host number than cowbirds if
PHYLO is correct.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
To assess the degree of genetic divergence among cowbird species, we used Lanyon's (1992
) DNA data to
compute Kimura two-parameter distances
(Kimura, 1980), which correct
for multiple basepair substitutions ("multiple hits"), for each
pair of taxa within the parasitic cowbirds. Distances were used in MEGA
(Kumar et al., 1994) to
construct a neighbor-joining tree with a topology identical to that of
Lanyon's maximum parsimony tree. To assess the extent of sequence divergence
among parasitic cuckoos, we sequenced 484 basepairs of the cytochrome b gene
from the common cuckoo (Cuculus canorus) and compared homologous
sequences from GenBank for the oriental cuckoo (C. saturatus; Chikuni
K et al., unpublished data; accession number 556489) and from Avise et al.
(1994) for the pallid cuckoo
(C. pallidus).
We determined the numbers of hosts used by parasitic cowbirds and cuckoos
from the literature (especially Johnsgard,
1997), even though some species in host lists are rare hosts whose
parasitism has little biological significance because they raise few or no
parasites. Indeed, we discuss various problems with the use of such lists
below, but we use this information nevertheless to make our analyses objective
and compatible with analyses used to formulate PHYLO.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Speciation, cowbird branching order, and specialization: an alternative to PHYLO
Partly because speciation events often involve dispersal to new regions, especially in birds (Chesser and Zink, 1994
; Mayr, 1963),
it is likely that the amount of time each cowbird species has been in contact
with its potential hosts is proportional to its branching position in the
cowbird phylogeny. In other words, the earliest species to diverge have
undergone the most prolonged coevolution with their particular array of
potential hosts and accordingly have become more specialized even in the
absence of cladogenesis. Therefore, greater specialization in the earliest
branching species is predicted by COEV and not in conflict with it. To assess
these hypothesized relationships among branching order, host numbers, and
speciation via dispersal, we constructed an area cladogram
(Figure 1) for parasitic
cowbirds using historical range distributions from Friedmann
(1929). The area cladogram
indicates a shift to an allopatric region with each subsequent split or
speciation event, most of which involved a northward expansion of the clade.
The split from M. rufoaxillaris to Scaphidura oryzivora, for
example, involved a range expansion from southern South America to northern
South America and Central America (Figure
1). Likewise, any ordering of the splits from the M.
aeneus to M. ater and M. bonariensis involves major
changes in geographic ranges (from Central America to North and South America
and the Caribbean). Our interpretation of this area cladogram is that
speciation events in the cowbird radiation generally involved dispersal to a
region where few or no cowbirds existed. Each cladogenic event was associated
with a cowbird species becoming sympatric with a new suite of relatively naive
host species, except that most of the area occupied by M. bonariensis
was already occupied by S. oryzivora
(Figure 1). However, this area
was still largely devoid of a cowbird capable of parasitizing a large number
of host species, because the huge size of S. oryzivora limits its
number of hosts (assuming S. oryzivora has always been large).
|
Parsimony and COEV versus PHYLO
PHYLO provides the most parsimonious explanation for the relation between
host number and the branching order of cowbird species. But how much more
parsimonious is PHYLO than COEV? Assume cowbirds have two levels of host
specialization: specialized, as characterized by M. rufoaxillaris and
S. oryzivora, each of which has 10 or fewer host species, and
generalized as in M. aeneus, M. ater, and M. bonariensis,
each of which has at least 80 hosts
(Friedmann et al., 1977;
Friedmann and Kiff, 1985;
Lowther, 1995). Under PHYLO,
the ancestral cowbird was a specialist, and the clade underwent one major
evolutionary change with regard to host numbers, a change from specialized to
generalized between the appearance of S. oryzivora and M.
aeneus (Figure 2a). Under
COEV (Figure 2b), the ancestral
cowbird was a generalist that gave rise to M. rufoaxillaris, which
then became specialized. A generalist then gave rise to S. oryzivora,
which also became specialized after splitting off from the lineage. Thus COEV
requires two evolutionary steps to produce the pattern seen today, whereas
PHYLO requires one step. The difference in number of minimum steps between
COEV and PHYLO would still be one if more levels of character states regarding
host numbers were used in the analysis (e.g., specialized, intermediate, and
generalized).
|
Biases inherent in published lists of hosts
The goal in assessing hypotheses such as COEV and PHYLO that deal with
specialization is to determine the degree of selectivity a parasite expresses.
Selectivity is more important than the number of known hosts because the
latter can be influenced by extraneous factors such as the amount of research
effort that has been applied to a parasite—host community and the number
of potential host species that are sympatric with a parasite. An important
determinant of sympatric host species is a parasite's range size. Published
literature is much more extensive for the North American M. ater than
for other cowbird species, all of which occur primarily or exclusively south
of the United States. If research effort is a bias, new hosts should become
known at a more rapid rate for these other cowbird species than for M.
ater, for which there were numerous data more than a century ago
(Bendire, 1893). Since Lanyon
(1992) proposed PHYLO using
published host lists, the known hosts of M. rufoaxillaris have
increased threefold, from one to three
(Mermoz and Reboreda, 1996;
Sick, 1993). Since
Friedmann's (1929) classic
host compilation, the list of known hosts has increased by 39% for M.
ater, from 158 in 1929 to 221 species at present
(De Gues and Best, 1991;
Lowther, 1993). In contrast,
hosts of M. bonariensis increased 145%, from 82 to 201 species, and
those of M. aeneus increased 413%, from 16 to 82 species, over the
same period (Friedmann and Kiff,
1985; Lowther,
1995). The proportion of known hosts added since Friedmann
(1929) is significantly
smaller in M. ater than in M. bonariensis (
2
= 41.2, p <.001) and M. aeneus (2 = 61.2,
p <.001).
Parasitic cowbirds are arranged as follows according to range size,
smallest to largest (Figure 1):
M. rufoaxillaris (3 host species), M. aeneus (82), S.
oryzivora (7), M. ater (221), and M. bonariensis (201).
Thus, host number correlates well with range size among parasitic cowbirds,
except for S. oryzivora, which has the third largest geographic range
and the fourth largest host number. However, this species' relatively large
body size, reflected in its common name (giant cowbird), restricts it to a
limited subset of hosts. The volume of S. oryzivora eggs is three to
five times that of the eggs of other parasitic cowbirds (based on measurements
in Friedmann, 1929) and few
passerine species are large enough to be suitable hosts.
Differentiating between COEV and PHYLO: the relative ages and host
numbers of the cowbird and cuckoo clades
The corrected DNA sequence divergence for cytochrome b of the entire
radiation of parasitic cowbirds averages 4.0%, and the maximum divergence
between the first species to branch off, the screaming cowbird (M.
rufoaxillaris) and the other four taxa averages only 5.7%. Fleischer et
al.'s (1998) calibration of
the chtochrome b nucleotide substitution rate for passerine birds (see also
Klicka and Zink, 1997) allows
an estimate of the time each cowbird species has coexisted with its hosts.
Applying the calibration of 1.5-2.0% divergence per million years to the
radiation of parasitic cowbirds indicates that the most specialized species,
M. rufoaxillaris, separated from the lineage leading to other
parasitic cowbirds 2.8-3.8 mya. The most recent divergence, which is between
the species that are the most generalized, the brown-headed and shiny cowbirds
(M. ater and M. bonariensis), dates to about 0.8-1.2
mya.
The cytochrome b data for cuckoos (Cuculus spp.) support a close
relationship between C. canorus and C. saturatus, which are
sympatric in Eurasia and have a corrected divergence of only 0.8 ±
0.4%. But C. pallidus, which occurs in Australia, has a corrected
divergence of 12.0 ± 1.7% with C. saturatus and 12.6 ±
1.8% with C. canorus. The sequence differences between C.
pallidus and its two congeners are more than twice as great as for the
entire cowbird radiation and indicate that cuckoos have been parasites for at
least 6.3-8.4 million years. Arbogast and Slowinski
(1998) argued that a
calibration of 1.5-2% substitutions per million years is 2.5 times too slow,
but these arguments have been rebutted
(Klicka and Zink, 1998).
Regardless of which calibration is correct, cuckoos in the subfamily Cuculinae
have likely been parasites at least twice as long as cowbirds have.
Given molecular data indicating that cuckoos have a longer history of
parasitism than cowbirds, PHYLO predicts that they should be more generalized
than cowbirds, whether it is based on time alone or on the number of
speciation events. COEV predicts the reverse (i.e., cuckoos should be more
specialized than cowbirds). Figure
3 shows frequency distributions of the numbers of known hosts for
cowbirds and cuckoos using data from various sources for cowbirds
(Friedmann and Kiff, 1985;
Lowther, 1995) and cuckoos
(Baker, 1942;
Becking, 1981;
Brooker and Brooker, 1989b;
Fry et al., 1988;
Johnsgard, 1997;
Wyllie, 1981). The five
cowbirds have a mean of 102.8 hosts and a median of 82, compared to 34.3 and
22.5 for the cuckoo species. The most generalized cuckoos are Cuculus
canorus and C. pallidus, with about 111 and 110 known host
species, respectively. In contrast, the two most generalized cowbirds, M.
ater and M. bonariensis, each have more than 200 hosts and are
therefore much more generalized than all 32 cuckoo species (p =.015,
Fisher's Exact test on 2 of 5 versus 0 of 32.).
Figure 3 includes all cuckoos
traditionally placed in the Cuculinae. Four species in the genus
Clamator may belong in another subfamily
(Aragon et al., 1999), but they
have little or no effect on overall results because host numbers for the
Clamator species (9-52) have nearly the same median, 22, as the
entire assemblage of 32 species, 22.5.
|
Total known host species (Figure
3) underestimate differences between cowbirds and cuckoos. Cuckoos
known to parasitize many species over their entire ranges typically parasitize
only one to six in any one region (Gibbs
et al., 2000; Higuchi,
1998; Nakamura et al.,
1998; Wyllie,
1981). In contrast, three of the five cowbirds (M. ater, M.
aeneus and M. bonariensis) commonly parasitize seven or more
species even at a single site (Carter,
1986; Mason,
1986a,
b;
Norris, 1947;
Robinson, 1992). Furthermore,
individual females typically parasitize multiple host species in generalist
cowbirds (Alderson et al.,
1999; Fleischer,
1985), but parasitize only a single species in cuckoos
(Gibbs et al., 2000;
Marchetti et al., 1998;
Wyllie, 1981). Contrary to
PHYLO, it is clear that cuckoos are more specialized than cowbirds at the
levels of species, populations, and individuals. Reliable data on host numbers
are not available for nearly 20 species of cuckoos, but the fragmentary data
(Johnsgard, 1997) for these
suggests that most or all specialize on a few host species, so their inclusion
would strengthen the difference between cowbirds and cuckoos.
Even more striking than the greater generalist tendency of cowbirds is
their greater variation in host number relative to that shown by cuckoo
species. The variance in cowbird host numbers
(Figure 3) is 10796.2, compared
to 967.6 for cuckoos. Host numbers are significantly (p <.0001)
more variable among cowbirds than among cuckoos (F ratio = 11.16).
This result, too, is contrary to PHYLO, which predicts that cuckoo species
should be more variable in host number. Also in conflict with the assumption,
under PHYLO, that host number has a strong phylogenetic signature is the fact
that the two cuckoo species with the largest and smallest numbers of known
hosts, Cuculus canorus with 111 species and C. gularis with
2, are sibling species that are barely distinguishable in the field except by
voice (Fry et al., 1988). If
two such similar congeners completely bracket the range of variation shown by
the remaining 30 cuckoo species in 5 genera, it is clear that host numbers are
too dynamic to elucidate ancestral states from present-day numbers.
Use of individual species as independent data points, as in the preceding Fisher's test, might seem to violate fundamental guidelines of the comparative approach because the characteristics of individual species within a clade may covary. However, this is unlikely to be a problem in the present case because host numbers in cowbirds are so labile that they bracket the range shown by all 32 cuckoo species (i.e., cowbird host numbers do not covary relative to the range of variation in the taxon to which they are being compared). Moreover, although it would be desirable to do this analysis on more than one old and one young clade of avian parasites, only these two clades, cuckoos and cowbirds, are suitable. DNA-based phylogenies are not available for other clades of parasites, some of which are too small (one to three species) to differentiate between COEV and PHYLO.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
An alternative model for the relation between branching order and specialization
PHYLO deals with position in a phylogeny and therefore with cladogenesis, whereas COEV deals with anagenesis (i.e., change within a lineage with no branching). Although historical in nature, COEV does not necessarily relate a brood parasitic species' degree of specialization to its position in a phylogeny. But how, then, can COEV explain the cowbird data, which seem to support PHYLO (i.e., a trend in which newly arising species seem to be progressively more generalized)?
First, as argued above, the number of hosts a brood parasite uses today may be different from its past numbers. One informative guide to identifying the primitive character state within a clade, comparison with an outgroup, is not possible with host numbers of brood parasites because nonparasitic outgroup species have no hosts. However, once speciation mechanisms are considered (Figure 1), COEV provides an explanation for the relation between current host numbers and branching order in cowbirds.
Our hypothesis for range expansions accompanying cladogenesis was well
supported by an area cladogram (Figure
1) and explains the phylogenetic pattern between host number and
branching order in cowbirds because speciation events generally involved
dispersal to a region where few or no cowbirds existed. The alternative of
vicariance events in a single, continuously distributed taxon does not fit the
tree or the geological history of the region. In contrast to our results,
Johnson and Lanyon (1999)
suggested that parasitic cowbirds show a lack of phylogenetic conservation of
biogeographic distributions because two species have had recent range
expansions and because the cowbirds are a mostly Neotropical group within a
clade of blackbirds that is primarily found in North America and the
Caribbean. However, the latter clade could have originated in the Neotropics
given the distribution of basal blackbirds
(Johnson and Lanyon, 1999),
and other blackbird clades, such as the meadowlarks, also have representatives
in North and South America (Lanyon and
Omland, 1999). Furthermore, the range expansions are due largely
to recent anthropogenic factors such as forest clearing and involve only the
most generalized cowbird species (Cruz et al.,
1989,
1998;
Rothstein, 1994).
PHYLO might occur if a parasite responds to hosts that develop defenses by
incrementally using additional host species
(Lanyon, 1992: 78). Continued
use of older, more well-defended host species would then result in an
increased number of hosts. However, there is nothing in PHYLO that explains
why, at each branching point, the lineage that gave rise to subsequent
branching events (i.e., new cowbird species) was more likely to become more
generalized than the lineage that showed no further branching. For example, if
the primitive state is specialization and generalization is achieved by
incremental additions of hosts, then the lineage that gave rise to the
present-day M. rufoaxillaris should be as much of a generalist as the
other four species because all have had the same amount of time to accrue the
incremental steps putatively needed to become a generalist. The same problem
exists with the other branching points. The failure of PHYLO to explain the
pattern it is based on is a serious weakness. In contrast, our proposed model
involving COEV and allopatric speciation provides the first causal explanation
for the host-use pattern that exists among cowbirds in that anagenesis within
lineages can produce a pattern among all taxa within the clade. Nevertheless,
the relationship between branching order and host species number in cowbirds
is in part fortuitous. Had M. ater colonized a continent with a
number of parasitic cuckoo species, it likely would be much more
specialized.
Unlike the case for cowbirds, COEV predicts a weak relationship, or none at all, between host number and the branching order of cuckoo species because cuckoos have been speciating for so long that many new species are likely to have appeared in regions that already contained other cuckoo species and other clades of brood parasites. Both of these complications are likely to have obscured relationships between branching sequence of cuckoo species and the level of defenses of potential hosts. In contrast, PHYLO predicts a correlation between branching order and host numbers of cuckoos. Although a complete phylogeny for cuckoos is lacking, the fact that sibling species (Cuculus canorus and C. gularis) bracket the range in host numbers shown by the entire cuckoo clade indicates that no clear phylogenetic pattern exists.
Instead of incremental host additions, a more likely basis for PHYLO might
be a relationship between ecological success and parasite density. Each
subsequent cowbird species may have speciated because it developed ecological
innovations that allowed it to both colonize a new region and to develop a
larger population. Large populations then may have provided pressures favoring
increases in numbers of host species. However, we stress that with time these
generalists are likely to become more specialized. This interpretation means
that both PHYLO and COEV may occur within a clade of parasites, with the
former preceding the latter. Low population size may explain the
specialization of the three Neotropical parasitic cuckoo species (subfamily
Neomorphinae) that specialize on high-quality hosts with domed,
predator-resistant nests (Johnsgard
1997).
Parsimony and COEV versus PHYLO
In distinguishing between COEV and PHYLO, the former has the advantage of
providing a cogent mechanistic explanation for the relation between phylogeny
and host number. Although it provides no cogent mechanism, PHYLO is more
parsimonious because it involves fewer evolutionary changes if one focuses
only on numbers of hosts. However, we have shown above
(Figure 2) that PHYLO is only
slightly more parsimonious than COEV, as the former requires one change to
produce the pattern seen today, whereas COEV requires two changes. Although
strict adherence to parsimony would lead one to endorse PHYLO over COEV, such
a tactic would inevitably lead to rejection of many cases of coevolution and
of such established phenomena as parallel evolution.
Furthermore, the focus on host number obscures an important fact. Whether a
parasite is a specialist or a generalist does not depend solely on genes
influencing host number. All specialist brood parasites have adaptations
specific to the particular host species they parasitize and therefore have
important differences among themselves. For example, M. rufoaxillaris
has a unique juvenile plumage that mimics that of its most common host and
that is different from the plumage of all other cowbirds (Fraga,
1978,
1979,
1998). The next most
specialized cowbird, S. oryzivora, also has unique features related
to its hosts such as a light-colored juvenile bill, eggs maculated with
scrawls, and preening of nest mates
(Friedmann, 1929;
Fraga, 1984;
Smith, 1968;
Orians, 1985;
Fleischer and Smith, 1992;
Robinson S, personal communication;
Skutch, 1996). Thus, a new
specialist branching off from an existing specialist will require evolutionary
changes even if there is little or no change in its host number. In other
words, sometime in its evolution, S. oryzivora had to undergo the
many host-related changes by which it differs from M. rufoaxillaris.
When all aspects of being a specialist are considered, the parsimony
difference between PHYLO and COEV is much less than appears to be the case
from a diagram (Lanyon, 1992:
Figure 1) showing only
branching position versus host number. Instead of a difference of one versus
two changes (Figure 2), the
difference is one less change for PHYLO out of the many changes both it and
COEV require to explain today's pattern of host use in cowbirds.
Intraspecific variation in host use by brood parasites
If the number of hosts a parasite uses is related more to the ecological
circumstances it faces than to its phylogenetic history, as predicted by COEV,
then brood parasites should show intraspecific variation in their use of
hosts, especially on spatial scales. In contrast, because PHYLO
(Lanyon, 1992) relates each
cowbird species' branching order to its ranking determined by current host
species number, it assumes that host use is stable over evolutionary time,
except during speciation, or that it is stable enough so that a ranking of
species based on current host numbers is the same as one based on host numbers
at the time each parasite speciated. In accord with COEV, extensive geographic
variation in host use occurs in both cowbirds and cuckoos.
Variation in host use occurs in even the most specialized cowbird, M.
rufoaxillaris. Despite M. rufoaxillaris' suite of adaptations
that make it highly adapted to one particular host species, M.
badius, there is frequent parasitism of the chopi blackbird
(Gnorimopsar chopi) in areas where M. badius is absent
(Fraga, 1996;
Sick, 1993) and occasional
parasitism of the brown and yellow marshbird (Pseudoleistes
virescens) where M. badius is present
(Mermoz and Reboreda, 1996).
Both of these additional hosts are very different in appearance from M.
badius, so parasitism of these species is not due to mistaken identity.
M. rufoaxillaris parasitism of other species may have gone unnoticed
in the past because field workers attributed its eggs to the sympatric
generalist M. bonariensis, which parasitizes numerous host species
and has similar eggs (Fraga,
1983; Friedmann,
1929). As more careful field work is done within the range of
M. rufoaxillaris, more hosts will likely be found, and this cowbird's
number of host species may come to surpass the seven known hosts of the next
species to branch off, S. oryzivora. Indeed, Pereya (in
Friedmann, 1963) listed six
additional hosts beyond the three noted above, but these records were not
accepted by Friedmann, who argued that the eggs cited by Pereya were M.
bonariensis eggs because of the belief that M. rufoaxillaris
parasitizes only one species, a belief now known to be incorrect.
It is clear that host use by M. rufoaxillaris is far more flexible
than appeared to be the case only a decade ago. Another example of the
flexible nature of host use is M. ater parasitism of the three
species of phoebes (Sayornis spp.), all of which place their nests
under a solid roof (rock overhangs or bridges), a habit shared by few other
North American passerines (Harrison,
1978). S. phoebe of eastern North America is the fifth
most parasitized of 221 known hosts, with more than 600 reported cases
(Friedmann, 1963,
Friedmann et al., 1977). In
contrast, there is not a single reliable case of parasitism on a western
congener, S. nigricans, even though both it and cowbirds reach their
highest abundances in riparian habitats
(Farmer, 1999). There are only
10 known cases of parasitism on the third species, S. sayi, which is
also limited to the western half of North America
(Friedmann, 1963;
Friedmann and Kiff, 1985;
Friedmann et al., 1977). All
three phoebes accept cowbird eggs
(Rothstein, 1986, unpublished
data), so eastern M. ater include a highly unusual nest type
(overhang nests) within their overall host niche, but western M. ater
do not.
Despite having a large list of host species summed over its entire range,
M. bonariensis shows different degrees of specialization in different
regions. It concentrates on cavity-nesting house wrens (Troglodytes
aedon) in northeastern South America and seems to parasitize few or no
other species in parts of Guyana and Suriname, even though this wren is an
uncommon host elsewhere (Friedmann,
1963). Elsewhere, this cowbird's main or exclusive host is a
grackle (Quiscalus lugubris) in an area of Venezuela
(Friedmann, 1963). In each of
two areas in Puerto Rico (Wiley,
1985), this cowbird concentrates most of its parasitism (> 90 %
of several hundred eggs) on only four host species. But in other regions,
numerous host species are used at single sites
(Fraga, 1978; Mason,
1986a,
b).
Other parasites also show spatial shifts in host use. In Europe and parts
of the Middle East, the great spotted cuckoo (Clamator glandarius) is
nearly exclusively parasitic on the black-billed magpie (Pica pica),
a species with an unusual domed nest
(Soler, 1990). In Israel and
Egypt, the great spotted cuckoo parasitizes a single species, the hooded crow
(Corvus corone), which has a typical cup-shaped nest
(Friedmann, 1964). At least 15
species of starlings (Sturnidae), which are cavity or tunnel nesters, and
other species of crows, are parasitized in much of Africa
(Arias-de-Reyna, 1998;
Friedmann, 1964). So this
cuckoo goes from one main host in the northern part of its range to 10 or more
hosts farther south.
These various examples of geographic variation show that intraspecific
variation in host use by some parasites approaches or exceeds the differences
in host use among some species of brood parasites. This is further evidence
that host use is too dynamic to allow present-day host numbers to reliably
reflect historical host numbers. Similarly, the range in numbers of hosts used
by two sibling species of cuckoos, Cuculus canorus and C.
gularis, exceeds the range shown by all other cuckoo species together.
Sympatric "gentes" of C. canorus that parasitize
different host species show only small mitochondrial DNA differences (Gibbs et
al., 1996,
2000), indicating that changes
in host use are frequent. Indeed, Nakamura et al.
(1998) described a major host
switch in the last several decades (see also
Brooke and Davies, 1987).
Additional problems with the use of host number as a character in a
cladogram
The use of published lists of known host species to assess specialization
obscures important aspects of a parasite's biology. A more appropriate measure
of specialization is selectivity, the extent to which a parasite uses
potential hosts with which it is sympatric. As shown above, lists of known
host species are strongly influenced by factors extraneous to degree of
selectivity such as the amount of research effort devoted to a parasitic
species and its range size. In addition, a parasite may not consider all
sympatric passerines as potential hosts because of body size constraints,
which is likely to be the case for S. oryzivora, as described above.
A list of known hosts can also misrepresent selectivity solely because it is
cumulative. If a specialized parasite switches from one host to another, as
documented by Nakamura et al.
(1998), both hosts will be in
a cumulative host list when, in fact, only one of them is parasitized at any
one time.
Thus it is not clear that a ranking of cowbird species based on host selectivity would be completely concordant with the divergence sequence (Figures 1 and 2) if it controlled for range and body size. For example, S. oryzivora might be as much of a generalist as the three later-branching cowbird species because it parasitizes most of the few passerines large enough to serve as hosts.
Clade age and host use in cowbirds and cuckoos
The demonstration that the Old World parasitic cuckoo clade (Cuculinae) is
at least twice as old as the New World parasitic cowbird clade and that the
cuckoos are more specialized in their host use clearly supports COEV over
PHYLO. Similarly, the greater interspecific variation in cowbird than in
cuckoo host numbers is inconsistent with PHYLO. Our comparison of cytochrome b
sequence divergence within cuckoos and cowbirds is conservative because the
cuckoo data come from three relatively undifferentiated congeners, whereas the
cowbird data represent the entire clade. Thus, data from the 11 other cuckoo
genera (Johnsgard, 1997)
should show that the disparity between ages of the cowbird and parasitic
cuckoo (Cuculinae) clades is greater than the twofold difference indicated by
our data. Aragon et al. (1999)
presented data on cytochrome b sequence divergence for eight species
traditionally included in the Cuculinae. These divergences ranged as high as
31.6%, but the largest divergences involved two species in the genus
Clamator, which Aragon et al. found to be a member of another clade.
If sequence data are restricted to the Cuculinae, as restructured by Aragon et
al.'s (1999) data, then the
cuckoo with the most divergent cytochrome b sequence, Cacomantis
flabelliformis, has 16.0-18.1% divergence with the other five species.
This indicates that Old World cuckoos have been parasites for as much as three
times as long as cowbirds. Furthermore, the entire Icterine radiation, of
which parasitic cowbirds make up only 5 of 97 species, is apparently
considerably younger than the group of these 5 cuckoos, as analyses of 59
species from all major subgroups within the Icterine showed a maximum
cytochrome b divergence of only 11.0% among lineages
(Lanyon and Omland, 1999).
Even a threefold disparity in ages of the cowbird and Cuculinae clades is a
likely underestimate because rates of sequence divergence slow down at higher
levels of divergence due to rapid saturation of amino acid replacements.
Furthermore, a much greater age for cuckoos than for cowbirds is in accord
with the DNA-DNA hybridization data of Sibley and Ahlquist (1991). These
authors identified Cuculiformes, the order to which parasitic cuckoos belong,
as an ancient group (see also Johnson et
al., 2000) that probably appeared in the Cretaceous.
In addition to their fewer hosts, there are further indications that
cuckoo-host interactions are more highly coevolved than those of cowbirds in
ways predicted by COEV. Nearly all species of cuckoos (Cuculinae) have eggs
that mimic the eggs of one or more of their most common host species
(Wyllie, 1981), as would be
expected from COEV if cuckoos have been parasites for a relatively long time.
In contrast, egg mimicry may occur in only one of the five cowbirds
(Smith, 1968), but even this
example is uncertain (Fleischer and Smith,
1992). Most species of cuckoos have eggs that are unusually small
for their body size (Payne,
1974; Wyllie,
1981) because they parasitize small hosts that discriminate
against large eggs (Davies and Brooke,
1988). In contrast, cowbirds lay eggs that are close to the size
predicted by the body size-egg size relationships in related nonparasitic taxa
(Rahn et al., 1988). The
nestlings of nearly all species of parasitic cuckoos evict host eggs and young
shortly after hatching and thereby monopolize all of the host's parental care
(Wyllie, 1981). Despite its
obvious adaptive value, cowbird nestlings do not kill off host young through
direct action, and some host young often fledge from parasitized nests. [There
is one report of a cowbird nestling ejecting a host nestling
(Dearborn, 1996), but this may
have been done passively.] These various comparisons of degrees of
specialization between brood parasitic cowbirds and cuckoos clearly support
COEV over PHYLO.
Examination of host numbers of three of the five other clades of parasitic
birds (the cuckoo-finch, Anomalospiza; the black-headed duck,
Heteronetta; the ground cuckoos, Neomorphinae) has little potential
for distinguishing between COEV and PHYLO because each has only one to three
species of obligate parasites. The two remaining clades, the viduine finches
(Viduinae) and the honeyguides (Indicatoridae), are more speciose than the
cowbirds, with at least 15 species each
(Johnsgard, 1997). Most
species in both clades are specialists with one to several hosts
(Fry et al., 1988;
(Klein et al., 1993;
Payne et al., 1993), with a
maximum of 49 known host species in one honeyguide
(Johnsgard, 1997). Given these
high levels of specialization, COEV predicts that these clades are older than
the cowbird clade, whereas PHYLO predicts the opposite
Macrogeographic variation in host use and host defenses
Besides the above support for COEV from comparisons among parasitic
lineages, further support comes from comparisons between regions, especially
for the hypothesis that there is a relation between number of parasitic
species in a region and level of host defenses. The African avifauna is
exposed to more than 30 species of parasitic birds in 3-5 lineages, depending
on taxonomy (Clamator plus rest of Cuculinae, Anomalospiza
plus Viduinae, and Indicatoridae), whereas there are only 3 in the Nearctic,
only 1 of which (M. ater) is widespread, and 7 in the Neotropics,
only 1 of which (M. bonariensis) is widespread and common
(Johnsgard, 1997;
Lack, 1968). As expected from
COEV, rejection of nonmimetic eggs is much more prevalent among African
passerines that are potential hosts than among Nearctic and Neotropical
species (Rothstein, 1990,
1992). In fact, most New World
passerines accept eggs strongly dissimilar from their own.
Similarly, the relatively small main island of Japan has four species of
Cuculus cuckoos, each specialized on a different set of one to six
host species (Higuchi, 1998;
Higuchi and Sato, 1984;
Lack, 1968;
Nakamura et al., 1998). Three
of these cuckoo species show weak to strong mimicry of host eggs in
coloration. The fourth, C. saturatus, mainly parasitizes a single
host whose domed nest may make discrimination via color difficult, although
the cuckoo's eggs mimic its host's in size
(Higuchi and Sato, 1984). The
egg mimicry by these cuckoos indicates that egg rejection is widespread in
Japanese passerines, an expectation borne out by experiments
(Nakamura et al., 1998).
Therefore, egg rejection is much more prevalent in Japanese birds than in New
World ones, in accord with COEV. Variation in egg rejection holds even for
potential hosts within a lineage. For example, egg rejection is uncommon or
absent in New World emberizine sparrows or buntings
(Mason, 1986a;
Rohwer and Spaw, 1988;
Rothstein, 1975b), although
many are parasitized by cowbirds, but is highly developed in the smaller
number of emberizine species that are potential cuckoo hosts in Japan
(Nakamura et al., 1998) and
Europe (Davies and Brooke,
1989a). Thus, COEV is consistent with both logical arguments and
available data when considering both the duration of parasite-host
interactions (previous subsection) and the numbers of parasites in different
regions.
|
ACKNOWLEDGEMENTS |
|---|
Helpful comments on various drafts of this manuscript were provided by M. Brooke, M. Christie, J. A. Endler, G. R. Kolluru, A. Kuris, K. Lafferty, J. T. Rotenberry, R. Sage, C. Sandoval, J. N. M. Smith, S. Sweet, J. Thompson, C. Tarr, R. Warner, R. M. Zink, and M. Zuk. Preparation of the manuscript was supported by National Science Foundation grant IBN 9728091.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Alcock J, 1993. Animal behavior: an evolutionary approach, 5th ed. Sunderland, Massachusetts: Sinauer Associates.
Alderson GW, Giggs HL, Sealy SG, 1999. Determining the reproductive behaviour of individual brown-headed cowbirds using micro-satellite DNA markers. Anim Behav 58: 895-905.[Web of Science][Medline]
Aragon S, Moller AP, Soler JJ, Soler M, 1999. Molecular phylogeny of cuckoos supports a polyphyletic origin of brood parasitism. J Evol Biol 12: 495-506.[Web of Science]
Arbogast BS, Slowinski JB, 1998. Pleistocene speciation and the mitochondrial molecular clock. Science 282: 1955.
Arias-de-Reyna L, 1998. Coevolution of the great spotted cuckoo and its hosts. In: Parasitic birds and their hosts, studies in coevolution (Rothstein SI, Robinson SK, eds). New York: Oxford University Press; 129-142.
Avise JC, Nelson WS, Sibley CD, 1994. Why one kilobase sequences from mitochondrial DNA fail to solve the hoatzin enigma. J Mol Phylogenet Evol 3: 175-184.
Baker ECS, 1942. Cuckoo problems. London: Witherby.
Becking JH, 1981. Notes on the breeding of Indian cuckoos. J Bombay Nat Hist Soc 78: 201-231.
Bendire CE, 1893. The cowbirds. Report of the U.S. National Museum for year ending June 30, 1893: 589-624.
Bolen GM, Rothstein SI, Trost C, 2000. Egg recognition in the yellow-billed magpie: evidence for long-term retention of host defenses in the absence of selection. Condor 102: 432-438.[Web of Science]
Braa AT, Moksnes A, Røskaft E, 1992. Adaptations of bramblings and chaffinches towards parasitism by the common cuckoo. Anim Behav 43: 67-78.
Brooke M de L, Davies NB, 1987. Recent changes in host usage by cuckoos Cuculus canorus in Britain. J Anim Ecol 56: 873-883.
Brooker MG, Brooker LC, 1989a. The comparative breeding behaviour of two sympatric species of cuckoos, Horsfield's bronze-cuckoo Chrysococcyx basalis and the shining bronze-cuckoo C. lucidus, in Western Australia: A new model for the evolution of egg morphology and host specificity in avian brood parasites. Ibis 131: 528-547.[Web of Science]
Brooker MG, Brooker LC, 1989b. Cuckoo hosts in Australia. Austral Zool Rev 2: 1-67.
Carter MD, 1986. The parasitic behavior of the bronzed cowbird in south Texas. Condor 88: 11-25.[Web of Science]
Chesser RT, Zink RM, 1994. Modes of speciation in birds: a test of Lynch's method. Evolution 48: 490-497.[Web of Science]
Cruz A, Post W, Wiley JW, Ortega CP, Nakamura TK, Prather JW, 1998. Potential impacts of cowbird range expansion in Florida. In: Parasitic birds and their hosts, studies in coevolution (Rothstein SI, Robinson SK, eds). New York: Oxford University Press; 313-336.
Cruz A, Wiley JW, Nakamura TK, Post W, 1989. The shiny cowbird Molothrus bonariensis in the West Indian region-biogeographical and ecological implications. In: Biogeography of the West Indies: past, present and future (Woods CA, ed). Gainesville, Florida: Sandhill Crane Press; 519-541.
Davies NB, 2000. Cuckoos, cowbirds and other cheats. New York: Academic Press.
Davies NB, Brooke M de L, 1988. Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav 36: 262-284.[Web of Science]
Davies NB, Brooke M de L, 1989a. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol 58: 207-224
Davies NB, Brooke M de L, 1989b. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. II. Host egg markings, chick discrimination and general discussion. J Anim Ecol 58: 225-236.
Davies NB, Brooke M de L, 1998. Coevolution between cuckoos and their hosts. In: Parasitic birds and their hosts, studies in coevolution (Rothstein SI, Robinson SK, eds). New York: Oxford University Press; 59-79.
Davies NB, Brooke M de L, Kacelnik A, 1996.
Recognition errors and probability of parasitism determine whether reed
warblers should accept or reject mimetic cuckoo eggs. Proc R Soc Lond
B 263:
925-931.
Dearborn DC, 1996. Video documentation of a brown-headed cowbird nestling ejecting an indigo bunting nestling from the nest. Condor 98: 645-649.[Web of Science]
De Geus DW, Best LB, 1991. Brown-headed cowbirds parasitize loggerhead shrikes: first records for family Laniidae. Wilson Bull 103: 504-506.
Farmer C, 1999. The density and distribution of brown-headed cowbirds: the Central Coastal California enigma. In: Research and management of the brown-headed cowbird in western landscapes (Morrison ML, Hall LS, Robinson SK, Rothstein SI, Hahn DC, Rich TR, eds). Stud Avian Biol 18: 62-67.
Fleischer RC, 1985. A new technique to identify and assess dispersion of eggs of individual brood parasites. Behav Ecol Sociobiol 17: 91-99.
Fleischer RC, Smith N, 1992. Giant cowbird eggs in the nests of two icterid hosts: the use of morphology and electrophoretic variants to identify individuals and species. Condor 94: 572-578.[Web of Science]
Fleischer RC, McIntosh CE, Tarr CL, 1998. Evolution on a volcanic conveyor belt: Using phylogeographic reconstructions and K-Ar-based ages of the Hawaiian Islands to estimate molecular evolutionary rates. Mol Ecol 7: 533-545.[Medline]
Fraga RM, 1978. The rufous-collared sparrow as a host of the shiny cowbird. Wilson Bull 90: 271-284.
Fraga RM, 1979. Differences between nestlings and fledglings of screaming and bay-winged cowbirds. Wilson Bull 91: 151-154.
Fraga RM, 1983. The eggs of the parasitic screaming cowbird (Molothrus rufoaxillaris) and its host, the baywinged cowbird (M. badius): is there evidence for mimicry? J Ornithol 124: 187-193.
Fraga RM, 1984. Bay-winged cowbirds (Molothrus badius) remove ectoparasites from their brood parasites, the screaming cowbirds (M. rufoaxillaris). Biotropica 16: 223-226.[Web of Science]
Fraga RM, 1996. Further evidence of parasitism of chopi blackbirds (Gnorimopsar chopi) by the specialized screaming cowbird (Molothrus rufoaxillaris). Condor 98: 866-867.[Web of Science]
Fraga RM, 1998. Interactions of the parasitic screaming and shiny cowbirds (Molothrus rufoaxillaris and M. bonariensis) with a shared host, the bay-winged cowbird (M. badius). In: Parasitic birds and their hosts: studies in coevolution (Rothstein SI, Robinson SK, eds). New York: Oxford University Press; 173-193.
Freeman S, Zink RM, 1995. A phylogenetic study of the blackbirds based on variation in mitochondrial DNA restriction sites. Syst Biol 44: 409-420.[Web of Science]
Friedmann H, 1929. The cowbirds: a study in the biology of social parasitism. Springfield, Illinois: Thomas.
Friedmann H, 1963. Host relations of the parasitic cowbirds. Proc US Natl Mus 233.
Friedmann H, 1964. Evolutionary trends in the avian genus Clamator. Smithson Misc Collect 146: 1-127.
Friedmann H, 1967. Alloxenia in three African species of Cuculus. Proc US Natl Mus 124: 1-13.
Friedmann H, Kiff LF, 1985. The parasitic cowbirds and their hosts. Proc West Found Vert Zool 2: 226-304.
Friedmann H, Kiff LF, Rothstein SI, 1977. A further contribution to knowledge of the host relations of the parasitic cowbirds. Smithson Contrib Zool 235.
Frumhoff PC, Reeve HK, 1994. Using phylogenies to test hypotheses of adaptation: a critique of some current proposals. Evolution 48: 172-180.[Web of Science]
Fry CH, Keith S, Urban EK, 1988. The birds of Africa, vol. III. London: Academic Press.
Gibbs HL, Brooke M de L, Davies NB, 1996. Analysis of genetic differentiation of host races of the common cuckoo Cuculus canorus using mitochondrial and microsatellite DNA variation. Proc R Soc Lond B 263: 89-96.[Medline]
Gibbs HL, Sorenson MD, Marchetti K, Brooke M de L, Davies NB, Nakamura H, 2000. Genetic evidence for female host-specific races of the common cuckoo. Nature 14407: 183-186.
Hamilton WJ III, Orians GH, 1965. Evolution of brood parasitism in altricial birds. Condor 67: 361-382.
Harrison C, 1978. A field guide to the nests, eggs and nestlings of North American birds. Cleveland, Ohio: Collins.
Higuchi H, 1998. Host use and egg color of Japanese cuckoos. In: Parasitic birds and their hosts: studies in coevolution (Rothstein SI, Robinson SK, eds). New York: Oxford University Press; 80-93.
Higuchi H, Sato S, 1984. An example of character release in host selection and egg colour of cuckoos Cuculus spp. in Japan. Ibis 126: 398-404.[Web of Science]
Hoover J P, Brittingham MC, 1993. Regional variation in cowbird parasitism of wood thrushes. Wilson Bull 105: 228-238
Hosoi A, Rothstein SI, 2000. Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim Behav 59: 823-840.[Web of Science][Medline]
Johnsgard PA, 1997. The avian brood parasites: deception at the nest. New York: Oxford University Press.
Johnson KP, Goodman SM, Lanyon SM. 2000. A phylogenetic study of the Malagasy couas with insights into cuckoo relationships. Mol Phylogenet Evol 14: 436-444.[Web of Science][Medline]
Johnson KP, Lanyon SM, 1999. Molecular systematics of the grackles and allies, and the effect of additional sequence (CYT B and ND2). Auk 116: 759-768.[Web of Science]
Kimura M, 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120.[Web of Science][Medline]
Klein NK, Payne RB, Nhalane MED, 1993. A molecular perspective on speciation in the brood parasitic Vidua finches. Proc VIII Pan-African Ornithol Congr 29-39.
Klicka J, Zink RM, 1997. The importance of recent ice
ages in speciation: a failed paradigm. Science
277: 1666-1669.
Klicka J, Zink RM, 1998. Pleistocene speciation and the mitochondrial molecular clock. Science 282: 1955.
Kumar S, Tamura K, Nei M, 1994. MEGA: molecular evolutionary genetics analysis, version 1.0. University Park: Pennsylvania State University.
Lack D, 1968. Ecological adaptations for breeding in birds. London: Methuen.
Lanyon SM, 1992. Interspecific brood parasitism in
blackbirds (Icterinae): a phylogenetic perspective. Science
255: 77-79.
Lanyon SM, Omland KE, 1999. A molecular phylogeny of the black-birds (Icteridae): five lineages revealed by cytochrome-B sequence data. Auk 116: 629-639.[Web of Science]
Lotem A, Nakamura H, Zahavi A, 1992. Rejection of
cuckoo eggs in relation to host age: a possible evolutionary equilibrium.
Behav Ecol 3:
128-132.
Lotem A, Nakamura H, Zahavi A, 1995. Constraints on egg discrimination and cuckoo-host co-evolution. Anim Behav 49: 1185-1209.
Lotem A, Rothstein SI, 1995. Cuckoo-host coevolution: from snapshots of an arms race to the documentation of coevolution. Trends Ecol Evol 10: 436-437.
Lowther PE, 1993. Brown-headed cowbird (Molothrus ater). In: The birds of North America, no. 47 (Poole A, Gill F, eds). Washington, DC: American Ornithologists' Union.
Lowther PE, 1995. Bronzed cowbird (Molothrus aeneus). In: The birds of North America, no. 144 (Poole A, Gill F, eds). Washington, DC: American Ornithologists' Union.
Marchetti K, 1992. Costs of host defence and the persistence of parasitic cuckoos. Proc R Soc Lond B 248: 41-45.[Medline]
Marchetti K, Nakamura H, Gibbs HL, 1998. Host-race
formation in the common cuckoo. Science
282: 471-472.
Mason P, 1986a. Brood parasitism in a host generalist, the shiny cowbird: I. The quality of different species as host. Auk 103: 52-60.[Web of Science]
Mason P, 1986b. Brood parasitism in a host generalist, the shiny cowbird: II. Host selection. Auk 103: 61-69.[Web of Science]
Mayr E, 1963. Animal species and evolution. Cambridge, Massachusetts: Belknap.
Mermoz ME, Reboreda JC, 1996. New effective host for the screaming cowbird. Condor 98: 630-632.[Web of Science]
Nakamura H, Kubota S, Suzuki R, 1998. Coevolution between the common cuckoo and its major hosts in Japan: stable versus dynamic specialization on hosts. In: Parasitic birds and their hosts: studies in coevolution (Rothstein SI, Robinson SK, eds). New York: Oxford University Press; 94-112.
Norris RT, 1947. The cowbirds of Preston Frith. Wilson Bull 59: 83-103.
Orians GH, 1985. Blackbirds of the Americas. Seattle: University of Washington Press.
Ortega CP, 1998. Cowbirds and other brood parasites. Tucson: University of Arizona Press.
Payne RB, 1974. The evolution of clutch size and reproductive rates in parasitic cuckoos. Evolution 28: 169-181.[Web of Science]
Payne RB, 1977. The ecology of brood parasitism in birds. Annu Rev Ecol System 8: 1-28.[Web of Science]
Payne RB, Payne LL, Nhalane MED, Hustler K, 1993. Species status and distribution of the parasitic indigo-birds Vidua in east and southern Africa. Proc VIIIth Pan-African Ornithol Congr 40-52.
Rahn H, Curran-Everett L, Booth DT, 1988. Eggshell differences between parasitic and nonparasitic Icteridae. Condor 90: 962-964.[Web of Science]
Robinson SK, 1992. Population dynamics of breeding Neotropical migrants in a fragmented Illinois landscape. In: Ecology and conservation of neotropical migrant landbirds (Hagan J III, Johnston DW, eds). Washington, DC: Smithsonian Institution Press; 408-418.
Rohwer S, Spaw CD, 1988. Evolutionary lag versus bill-size constraints: a comparative study of the acceptance of cowbird eggs by old hosts. Evol Ecol 2: 27-36.
Rothstein SI, 1975a. Evolutionary rates and host defenses against avian brood parasitism. Am Nat 109: 161-176.[Web of Science]
Rothstein SI, 1975b. An experimental and teleonomic investigation of avian brood parasitism. Condor 77: 250-271.[Web of Science]
Rothstein SI, 1976. Cowbird parasitism of the cedar waxwing and its evolutionary implications. Auk 93: 498-509.[Web of Science]
Rothstein SI, 1982a. Mechanisms of avian egg recognition: which egg parameters elicit responses by rejecter species? Behav Ecol Sociobiol 11: 229-239.[Web of Science]
Rothstein SI, 1982b. Successes and failures in avian egg and nestling recognition with comments on the utility of optimality reasoning. Am Zool 22: 547-560.
Rothstein SI, 1986. A test of optimality: egg recognition in the eastern phoebe. Anim Behav 34: 1109-1119.
Rothstein SI, 1990. A model system for coevolution: avian brood parasitism. Annu Rev Ecol System 21: 481-508.[Web of Science]
Rothstein SI, 1992. Brood parasitism, the importance of experiments and host defences of avifaunas on different continents. Proc VIIth Pan-African Ornithol Congr 521-535.
Rothstein SI, 1993. An experimental test of the Hamilton-Orians hypothesis for the origin of avian brood parasitism. Condor 95: 1000-1005.[Web of Science]
Rothstein SI, 1994. The brown-headed cowbird's invasion of the Far West: history, causes and consequences experienced by host species. In: A century of avifaunal change in western North America (Jehl JR Jr, Johnson NK, eds). Stud Avian Biol 15: 301-315.
Rothstein SI, 2001. Relic behaviors, coevolution and the retention versus loss of host defenses after episodes of avian brood parasitism. Anim Behav 61: 95-107.[Web of Science][Medline]
Rothstein SI, Robinson SK (eds), 1998. Parasitic birds and their hosts: studies in coevolution. New York: Oxford University Press.
Schluter D, Price T, Mooers AØ, Ludwig D, 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51: 1699-1711.[Web of Science]
Sealy SG, 1996. Evolution of host defenses against avian brood parasitism: implications of puncture-ejection by a small passerine. Auk 113: 346-355.[Web of Science]
Sibley CG, Ahlquist JE, 1990. Phylogeny and classification of birds: a study in molecular evolution. New Haven, Connecticut: Yale University Press.
Sick H, 1993. Birds in Brazil. Princeton, New Jersey: Princeton University Press.
Skutch AF, 1996. Orioles, blackbirds, and their kin. Tucson: University of Arizona Press.
Smith NG, 1968. The advantage of being parasitized. Nature 219: 690-694.[Medline]
Soler M, 1990. Relationships between the great spotted cuckoo Clamator glandarius and its corvid hosts in a recently colonized area. Ornis Scand 21: 212-223.
Soler M, Møller AP, 1990. Duration of sympatry and coevolution between the great spotted cuckoo and its magpie host. Nature 343: 748-750.
Soler JJ, Møller AP, 1996. A comparative
analysis of the evolution of variation in appearance of eggs of European
passerines in relation to brood parasitism. Behav Ecol
7: 89-94.
Swofford DL, 1993. PAUP, phylogenetic analysis using parsimony, version 3.1.1. Champaign: Illinois Natural History Survey.
Thompson JN, 1994. The coevolutionary process. Chicago: University of Chicago Press.
Wiley JW, 1985. Shiny cowbird parasitism in two avian communities in Puerto Rico. Condor 87: 165-176.[Web of Science]
Wyllie I, 1981. The cuckoo. New York: Universe Books.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  O. Kruger, M. D. Sorenson, and N. B. Davies Does coevolution promote species richness in parasitic cuckoos? Proc R Soc B, November 7, 2009; 276(1674): 3871 - 3879. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. C De Marsico and J. C Reboreda Differential reproductive success favours strong host preference in a highly specialized brood parasite Proc R Soc B, November 7, 2008; 275(1650): 2499 - 2506. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Roskaft, F. Takasu, A. Moksnes, and B. G. Stokke Importance of spatial habitat structure on establishment of host defenses against brood parasitism Behav. Ecol., September 1, 2006; 17(5): 700 - 708. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. E. Mermoz and J. F. Ornelas Phylogenetic analysis of life-history adaptations in parasitic cowbirds Behav. Ecol., January 1, 2004; 15(1): 109 - 119. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||