Behavioral Ecology Vol. 12 No. 2: 128-133
© 2001 International Society for Behavioral Ecology
The evolution of obligate interspecific brood parasitism in birds
Laboratoire d'Ecologie, CNRS UMR 7625, Université Pierre et Marie Curie, Bât. A., 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France
Address correspondence to M. Robert. E-mail: mrobert{at}snv.jussieu.fr .
Received 26 July 1999; revised 9 November 1999; accepted 10 April 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONDISCUSSIONREFERENCES |
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We present a simple analytical model to investigate the conditions for the evolution of obligate interspecific brood parasitism in birds, based on clutch size optimization, when birds can lay more eggs than their optimal clutch size. The results show that once intraspecific parasitism has appeared (i.e., females start to spread their eggs over their own and other nests) the evolutionarily stable number of eggs laid in its own nest decreases. Two possible ESSs exist: (1) either the evolutionarily stable number of eggs laid in its own nest is larger than zero, and a fraction of the total number of eggs is laid parasitically (i.e., intraspecific parasitism); and (2) either the evolutionarily stable number of eggs laid in its own nest is zero and all eggs are laid parasitically. Since all females lay parasitically, this could favor the evolution of obligate interspecific brood parasitism. The key parameter allowing the shift from intraspecific to obligate interspecific parasitism is the intensity of density-dependent mortality within broods (i.e., nestling competition). Strong nestling competition, as in altricial species, can lead to an ESS where all eggs are laid parasitically. Altricial species are, therefore, predicted to evolve more easily toward obligate interspecific parasitism than precocial species. These predictions fit the observed distribution of brood parasitism in birds, where only one species out of 95 obligate interspecific parasites exhibits a precocial mode of development. Different nestling survival functions provided similar findings (i.e., obligate brood parasitism is more likely to evolve in altricial species), suggesting that these results are robust with respect to the main assumption of the model.
Key words: clutch size, intraspecific nest parasitism, interspecific nest parasitism, nestling survival, parental care.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONREFERENCES |
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Brood parasitism can take two forms in birds (Lack, 1968
;
Payne, 1977b;
Yom-Tov, 1980;
Rothstein, 1990): females lay
in the nest of a conspecific (i.e., intraspecific parasitism), or in the nest
of a female belonging to a different species (i.e., obligate interspecific
parasitism). Intraspecific nest parasitism is much more common in birds that
have self-feeding young (i.e., precocial species)
(Rohwer and Freeman, 1989),
whereas obligate interspecific parasitism essentially occurs in species where
young need to be fed by parents (i.e., altricial species)
(Lyon and Eadie, 1991).
How did obligate interspecific parasitism evolve, and why are there many
more obligate interspecific parasites among altricial birds as compared to
precocial species? The evolution of brood parasitism in birds has attracted
considerable attention from evolutionary biologists and several hypotheses
have been put forward to explain the origin and maintenance of brood parasitic
behavior. Hamilton and Orians
(1965) suggested that brood
parasitism could have evolved as a consequence of nest loss during the egg
laying period and the physiological need to lay committed eggs would have
promoted parasitic behavior. However, empirical studies have provided mixed
support for this hypothesis (see Rothstein,
1993,
1994;
Stouffer and Power, 1991;
Yezerinac and Dufour, 1994).
Further theoretical work has focused on the ancestral form of parasitism,
whether interspecific parasitism has evolved via intraspecific parasitism, or
directly from non-parasitic individuals. Using a quantitative genetic model,
Yamauchi (1995) suggested that
intraspecific parasitism might be the original form of parasitism, and that
obligate interspecific parasitism should evolve if the decline in survival of
parasitic eggs is smaller than the cost of interspecific parasitism. Recently,
the view of an ancestral intraspecific parasitism has been challenged. Under
the assumption of strong nestling competition, a parasite that would exploit a
smaller host could experience greater reproductive success because of the
size-advantage of its offspring
(Slagsvold, 1998). None of
these hypotheses explicitly addresses the observed distribution of brood
parasitism among altricial and precocial birds. Lyon and Eadie
(1991) have proposed a
possible explanation of such a distribution. They suggested that the rarity of
obligate brood parasitism in precocial birds could be the consequence of
little fitness gain (in terms of fecundity) via obligate brood parasitism, and
that such small gain could easily be obtained via facultative parasitism. Lyon
and Eadie (1991) focused on
the factors that could influence whether a precocial species became an
obligate interspecific parasite, once parasitism has appeared, but does not
consider factors promoting the origin of parasitism.
Here we present a simple mathematical model based on clutch size optimization, which explains how obligate interspecific brood parasitism could evolve, and why this behavior is almost only present in altricial species.
A simple clutch size optimization model
Life history theory assumes that phenotypes are molded by natural selection
in order to optimize individual fitness
(Stearns, 1992). Females of
several bird species are physiologically able to lay more eggs than they
actually produce and incubate (Kennedy,
1991; Klomp, 1970;
Murphy and Haukioja, 1986;
Winkler and Walters, 1983).
Because nestling mortality often increases with the number of eggs laid,
natural selection is expected to result in an optimal clutch size which
maximizes the number of offspring produced
(Lack, 1947). If we assume
that the relationship between the number of eggs laid, x, and the
survival probability of nestlings, s1 (x), has a
linear form
 | (1\mathrm|<|a|>|) |
 | (1\mathrm|<|b|>|) |
(x) =
s1(x) = x(1 - ax)
(Figure 1). In the absence of
brood parasitism, the optimal clutch size xL (Lack's
clutch size) which maximizes the number of fledged young is 1/2a
(Andersson, 1984).
|
Let n be the potential maximum number of eggs that a female can
produce under the current environmental conditions (i.e., female potential
egg-laying capacity). If xL (Lack's clutch size) is less
than the female egg-laying capacity (n), as observed in several bird
species (Kennedy, 1991;
Klomp, 1970;
Lack, 1947), a parasitic
female that lays xL eggs in her nest and y eggs
in nests of conspecifics (xL + y being 
n) would have greater reproductive success than non-parasitic
females, under the assumptions that: (1) the energetic cost of laying eggs is
lower than the fitness increment expected from parasitic eggs, and (2) there
is no host defense. We considered that parasitic eggs are laid in different
nests, that is to say that each female parasitizes y different nests.
We also assumed that all parasitic eggs are uniformly distributed among nests
(i.e., all nests receive the same average number of parasitic eggs).
The reproductive success of a female laying x eggs in her nest and
y in the nests of conspecifics in a population where all females lay
x' eggs in their nest and y' in the nests of
conspecifics is:
 | (2) |
; Lyon,
1993,
1998). Here we suppose
g greater than zero and smaller than one.
As the reproductive success of individuals following a given strategy will
be affected by the strategies adopted by the other individuals, we used a game
theory approach. A strategy can be considered evolutionarily stable if, when
adopted by all individuals in a population, can not be invaded by any mutant
strategy (Maynard Smith,
1982). Then, the strategy "laying x*
eggs in its own nest, y* in the nests of
conspecifics" can be considered as an evolutionarily stable strategy if
(x*,y*,
x*,y*) > (x,y;
x*,y*) for all sets (x,y)
(x*,y*).
If (x*,y;
x*,y*) is the reproductive success of
a mutant female (x*,y) in a
(x*,y*) population, the stability
requires that (Maynard Smith,
1982)
 | (3\mathrm|<|a|>|) |
 | (3\mathrm|<|b|>|) |
The reproductive success of (x*, y) and
(x, y*) mutants in a (x*,
y*) population are respectively:
 | (4) |
 | (5) |
(x*,y;x*,y*)
is a growing function of y and y lies between 0 and n -
x, the reproductive success () reaches a maximum when the total
number of eggs laid is n (x + y = n). Given that
the number of eggs that can be laid is not infinite, there is a trade-off
between the number of eggs that a female lays in her nest and the number of
eggs laid in conspecific nests.
Thus the resident strategy is to lay x* eggs in its own
nest and n - x* in conspecific nests, whereas the mutant
strategy is to lay x eggs in its own nest and n - x in
conspecific nests. Replacing y* of the mutant by n -
x and y* of the resident by n -
x* in Equation 5 gives:
 | (6) |
 |
Thus the evolutionarily stable number of eggs laid in its own nest
(x*) is greater than zero. At equilibrium, each female
lays some of their eggs in their nests and some parasitically. In this case,
intraspecific parasitism is a stable state. Note that x*
is smaller than the optimal clutch in the absence of parasitism (given that
n > 1/2a, then x* < (1 -
g) (1/a - 1/2a) < (1/a - 1/2a)
and thus x* < 1/2a). The model, therefore,
predicts that intraspecific nest parasitism should favor a reduction in the
number of eggs a parasitic female lays in her own nest. This result is in
agreement with the predictions of a recent graphical model on clutch size and
intraspecific brood parasitism (Lyon,
1998). Empirical evidence supporting this prediction has been
provided for the European starling (Sturnus vulgaris)
(Power et al., 1989), the
goldeneye (Bucephala clangula)
(Andersson and Eriksson, 1982),
and the American coot (Fulica americana)
(Lyon, 1998).
Second, 1/a n. In this case, the ESS
(x*,y*) is to lay
x* = 0 in its own nest and y* =
n parasitically.
This means that it pays to lay all eggs parasitically. The value of the
parameter y* when x* = 0 (i.e.,
n 
1/a) corresponds to the critical value where each
female achieves zero fitness. Whatever the mutant (x,y*),
we obtain (x*,y*;
x*,y*) = (x,y;
x*,y*) = 0.
This is a paradoxical finding, but similar phenomena are well known by
economists. For instance, a sole owner can manage a resource to maximize
sustainable profit but the "economic rent is dissipated" in the
absence of sole ownership (Clark, 1976, in
May et al., 1991). This can
lead to situations where the marginal rate of return is zero; everyone loses,
locked into the perverse logic of commons
(Hardin, 1968).
Two outcomes are then conceivable. The first one is population extinction, because none of the eggs laid would produce fledged young. The second outcome could be the appearance of obligate interspecific parasitism. Given that females should lay all their eggs in other nests, this could favor the loss of nest-making habits and promote the shift toward obligate interspecific parasitism. According to this scenario, intraspecific parasitism would be the ancestral form of brood parasitism.
The results of the model also show that brood parasites (both intra- and
interspecific) should increase the total number of eggs laid (because
x* + y* is always higher than
xL), depending on resource availability. In agreement with
this prediction, parasitic cuckoos, cowbirds and weavers lay many more eggs
per season than their non-parasitic relatives (Payne,
1973,
1976,
1977a;
Scott and Ankney, 1980).
Intraspecific parasites also have larger fecundity compared to non-parasitic
females, although the gain in fecundity due to parasitism is smaller than in
obligate interspecific parasites (e.g.,
Lyon, 1998).
The evolution of obligate interspecific parasitism (x*
= 0) could, thus, depend on two parameters: a (i.e., the slope of the
regression of nestling survival on clutch size) and n (i.e., the
maximum number of eggs that can be laid under the current environmental
conditions). Parental care in birds ranges from absence to complete attendance
and feeding (Clutton-Brock,
1991). Absence of parental care is rare and the vast majority of
bird species show various degrees of parental care, such as incubation,
brooding, defense and feeding of young. As already observed by Lack
(1947), feeding is likely to
be the most costly care provided by parents. Therefore, an increase in brood
size has probably a stronger effect on nestling survival in species where
parents feed their young (i.e., altricial species) as compared to species
where they do not (i.e., precocial species). In other words, the parameter
a is probably smaller in precocial than altricial species and,
therefore, 1/aalt < 1/aprec.
The maximum number of eggs that can be laid under the current environmental
condition (n) is the other parameter potentially involved in the
evolution of obligate interspecific parasitism. We are not aware of any
studies that have extensively investigated egg-laying capacity in precocial
and altricial species. Eggs of precocial species are usually larger (for a
given body size) than eggs of altricial birds and should therefore be more
costly to produce (Winkler and Walters,
1983). One could suppose that egg-laying capacity is more
constrained by available resources in precocial species. However, altricial
birds are involved in extremely high energy demanding activities during
feeding of young, which could also constrain maximum egg-laying capacity. Many
species produce more developing follicles than eggs and therefore have the
potential to be indeterminate layers, although not all of them exhibit
indeterminacy (Kennedy, 1991).
A review of egg-laying patterns in birds showed that there is no difference in
the frequency of determinate and indeterminate layers between altricial and
precocial species (Kennedy,
1991). As a consequence of these different phenomena, it seems
plausible, as a first approximation, to consider n to be similar in
altricial and precocial species.
If n is constant and a is higher in altricial species, then the threshold egg-laying capacity beyond which x* equals zero should be lower for altricial than for precocial species. Consequently, this simple model suggests that obligate interspecific parasitism is more likely to evolve in altricial species.
Changing the assumptions for the nestling survival function
The previous results were derived under the assumption of a linear
relationship between the number of young fledged and the number of eggs in the
nest. Because the nestling survival function is the most crucial parameter of
the model, we considered another function and calculated, as in the previous
section, the evolutionarily stable clutch size. The nestling survival function
considered here is:
 | (7) |
; Yves,
1989). In the absence of parasitism, female reproductive success
is defined by (x) = x s2(x) and
the optimal clutch size is 1/r
(Figure 1). As for the previous model, if the female potential egg-laying capacity (n) is larger than the optimal clutch size in the absence of parasitism (n > 1/r), then it pays to spread the eggs over its own and other nests.
The reproductive success of a female (x,y) in a population where
all females lay x' eggs in their nest and y' in
the nests of conspecifics is:
 | (8) |
 | (9) |
 | (10) |
is a growing function of y,
and y lies between 0 and n - x, the reproductive success
reaches a maximum at y = n - x.
Equation 10 becomes:
 | (11) |
 | (12) |
). The evolutionarily stable number of eggs laid in its own nest (x*) equals zero only when g is one, that is when parasitic and non-parasitic eggs have the same hatching and fledging probabilities. In this case, it is easy to understand why a female should lay all her eggs in nests of other individuals. When g is smaller than one, x* can never be zero. However, since the number of eggs laid in the own nest is a discrete quantity, we can assume that when x* is lower than one, the evolutionarily stable number of eggs laid in its own nest is zero.
As for the previous model two outcomes are, then, possible (for 0 <
g < 1): First, if g + r 1, the
evolutionarily stable number of eggs laid in its own nest
(x*) is greater than zero. At equilibrium, each female
lays an average of x* eggs in her nest and n -
x* parasitically. Since x* is smaller than
the optimal clutch size in the absence of parasitism (x*
< 1/r) a clutch size reduction is predicted to be an adaptive
response to intraspecific parasitism, the magnitude of this reduction
depending on the value of g. This is similar to the result obtained
with a linear nestling survival function.
Second, if g + r > 1, then x* < 1 and the evolutionarily stable number of eggs laid in its own nest is zero (i.e., this quantity cannot be lower than one and higher than zero). This means that it pays to lay all eggs parasitically. Similar to the previous model, if x* = 0, two outcomes are conceivable: (1) population extinction; and (2) the evolution toward obligate interspecific parasitism.
Optimal clutch size (i.e., 1/r) is generally higher for precocial
than for altricial species (Lack,
1968; Winkler and Walters,
1983), which implies that r is generally larger for
altricial species. If r is larger for birds with an altricial mode of
development (and assuming that g is similar in altricial and
precocial species) then g + r is more likely to be higher
than one in altricial birds. As shown above, when g + r >
1, the evolutionarily stable number of eggs laid in its own nest
(x*) is smaller than one. Therefore, this model also
suggests that obligate interspecific parasitism is more likely to evolve via
intraspecific parasitism in altricial species.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONREFERENCES |
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Obligate interspecific parasitism and intraspecific nest parasitism have evolved independently several times in birds. Obligate interspecific parasitism has been reported in 95 species belonging to six families (Johnsgard, 1997
), among which
only one species has a precocial mode of development (the duck Heteronetta
atricapilla). On the contrary, conspecific and facultative interspecific
parasitism is disproportionately more common among precocial bird that have
self-feeding young compared to species which feed their offspring
(Lyon and Eadie, 1991;
Rohwer and Freeman, 1989). In
birds, there are many more altricial than precocial species; therefore the
rarity of precocial obligate brood parasites could be the mere consequence of
the relative abundance of these two modes of development in birds (Payne,
1997a). However, this hypothesis has been rejected because the frequency of
obligate brood parasitism in precocial birds is lower than expected on the
basis of the relative abundance of a precocial mode of development
(Lyon and Eadie, 1991).
Several hypotheses have been suggested to explain the evolution of obligate
interspecific parasitism in birds. Some authors have suggested that nest
parasitism is the consequence of a degeneration of nesting instincts or the
failure to synchronize nest-building and egg laying (see
Hamilton and Orians, 1965 for
a review). Hamilton and Orians
(1965) provided an alternative
route which may have led to interspecific parasitism. They suggested that
brood parasitism may have evolved through tendencies of certain species to lay
in the nests of other females, either as a consequence of nest destruction, or
accidental placement of eggs. However, the repeated observation of parasitic
females incubating their own eggs weaken the argument of an
"accidental" origin of brood parasitism, and support the view that
brood parasitism may be a reproductive strategy
(Brown and Brown, 1988). More
recently, two models have addressed the question concerning the evolutionary
pathways favoring the transition between intra- and interspecific parasitism
(Yamauchi, 1995) and between
facultative and obligate interspecific parasitism
(Lyon and Eadie, 1991). In a
quantitative genetic model Yamauchi
(1995) has shown that, under
the assumption of ancestral intraspecific parasitism, obligate interspecific
parasitism can evolve if the marginal decline in the survival rate of
parasitic eggs in nests of different species is lower than the cost of
parasitism. The transition between facultative and obligate interspecific
parasitism has been investigated by Lyon and Eadie
(1991), who argued that
because precocial species gain little in terms of fecundity from obligate
parasitism in precocial species, this strategy should evolve only in altricial
species. Surprisingly, little attention has been paid to how changes in
optimal clutch size as a response to intraspecific parasitism might lead to
stable obligate brood parasitism. To our knowledge, our simple model is the
first showing that: (1) Obligate brood parasitism could have evolved as a
consequence of subsequent adjustments of clutch size in response to
intraspecific parasitism, and (2) obligate brood parasitism is more likely to
be an evolutionary end point in altricial than in precocial species. These
conclusions rest on the consideration that when the evolutionarily stable
strategy is to lay all eggs parasitically, females stop to built a nest and
become obligate interspecific parasites. This argument is, by nature,
untestable and might appear more like an unsupported speculation. However, we
would like to stress that this speculative argument is inherent to all models
on the evolution of brood parasitism. Regardless of the possible costs and
benefits of this reproductive strategy we have to admit that, at a given point
in time, parasitic individuals lost their ability to build a nest and became
obligate interspecific parasites.
The time needed to evolve toward interspecific parasitism will depend on the length of the different stages of this evolutionary race: (1) all females adopt an optimal clutch size; (2) parasitic strategy appears and spreads, laying the optimal clutch size in its own nest and some additional eggs in other nests; (3) there is a cost of reduced nestling success because all individuals received parasitic eggs, thus the best outcome is to reduce the number of eggs laid in its own nest; and (4) when this reduction is complete, a new strategy can appear where individuals lay all their eggs in the nests of other species. Obviously, the duration of each of these steps is difficult to predict and probably depends on whether the evolution of clutch size requires genetic changes or is based on phenotypic adjustments.
Our model is essentially based on the assumptions that birds lay a lower
number of eggs than their maximum egg-laying capacity, and nestling survival
decreases with increasing brood size. Both assumptions have received
supportive evidence (Dijkstra et al.,
1990; Kennedy,
1991; Klomp, 1970;
Lack, 1947;
Lindén and
Møller, 1989; Murphy
and Haukioja, 1986; Winkler
and Walters, 1983). Clutch size manipulations have been performed
in several altricial bird species. Lindén and
Møller (1989) and
Dijkstra et al. (1990) have
reviewed published studies on clutch size manipulation in altricial species,
and showed that most studies (28 out of 44 studies) found a reduction of
nestling survival in enlarged broods (in no study survival was better in
enlarged broods). On the contrary, clutch size manipulations involving species
with a precocial mode of development are scarce. The main reason for the
paucity of such experiments is the difficulty to measure survival of young,
because they generally leave the nest soon after hatching. Furthermore, on a
theoretical ground one could assume that if the decrease in nestling survival
with increasing brood size in altricial birds is the result of limited ability
to provision the young, then nestling survival should be independent of brood
size in precocial species. However, as mentioned above, precocial young also
need parental care, potentially limiting nestling survival. Experimental
evidence (Andersson and Eriksson,
1982; Eadie and Fryxell,
1992; Lessells,
1986; Safriel,
1975) showed an adverse effect of increasing brood size on young
survival (but see also Dow and Fredga,
1984; Lepage et al.,
1998; Milonoff et al.,
1995). Although several experiments both on altricial and
precocial species have reported a reduction of survival rate for enlarged
brood, reducing clutch size does not necessarily result in an increase of
nestling survival compared to control unmanipulated clutches
(Dijkstra et al., 1990). In
this case, it would be more realistic to consider the following nestling
survival function:
- For x between 0 and the Lack's clutch size, nestling survival rate
is constant s(x) = k
- For x larger than the Lack's clutch size, nestling survival
decreases linearly as the clutch size increases s(x) = 1 -
ax (for x > 1/2a). It is easy to show that
considering this nestling survival function provides the same results as when
assuming a linear negative relationship between clutch size and nestling
survival. Therefore, although the relationship between nestling survival and
brood size could differ between altricial and precocial species, our model
suggests that obligate brood parasitism is more likely to evolve in altricial
species independently of the nestling survival function considered.
Another assumption of the second model is that when x* is lower than one, the evolutionarily stable number of eggs laid in its own nest is zero. This might not be necessarily the case and laying in its own nest might still be the ESS for values of x* lower than one. To determine the integer number of eggs a female should lay when x* is a real between 0 and 1 needs complex analysis. This is a general problem arising when modeling discrete quantities (such as clutch size) with continuous functions. Nonetheless, this does not change our results. Even though the threshold x* value below which all eggs should be laid parasitically is lower than one, one can still easily demonstrate that altricial species have higher likelihood to evolve toward obligate brood parasitism compared to precocial species.
Obligate interspecific brood parasitism has appeared several times in birds, and about 1% of species has adopted this reproductive strategy. Given the potential benefits of brood parasitism, in terms of reduced parental care, one could have expected brood parasitism to be more widespread. However, several constraints can substantially reduced the reproductive success of obligate interspecific parasites. Costs of parasitism can take several forms, including inadequate parental care provided by foster parents (in terms of incubation efficiency, food quality, nestling competition), imprinting on a wrong species (which could have negative effects on mate selection), and host defense. For the sake of simplicity, our model included only one cost of parasitism (i.e., the reduction of survival of eggs laid parasitically) and we considered that this reduction was never complete. However, in most instances eggs laid parasitically could have zero survival (e.g., due to host unsuitability), which could explain why brood parasitism still remains a relatively rare reproductive strategy in birds. Host availability and time needed to search for host nests might also be important costs associated with brood parasitism.
In conclusion, we have shown that the effect of intraspecific parasitism on
optimal clutch size could lead to obligate interspecific parasitism, and that
this is more likely to happen in species with an altricial mode of
development. Other groups of animals, like arthropods, have different modes of
development and both intra- and interspecific brood parasitism
(Choe and Crespi, 1997;
Kaitala and Miettinen, 1997).
Comparative studies across these taxa might prove useful as an independent
test of the predictions provided by our model on the evolution of
interspecific brood parasitism.
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ACKNOWLEDGEMENTS |
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We thank Minus van Baalen, Thierry Boulinier, Mark Kirkpatrick, Anders Pape Møller, and Tony Ives for improving a previous version of the manuscript. This work has been supported by the Ministère de l'Education Nationale and the Programme 98N62/0110 "Environnement, Vie et Société" of the CNRS.
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