Philip L. G. Birget, Stephen D. Larcombe. 2015: Maternal effects, malaria infections and the badge size of the house sparrow. Avian Research, 6(1): 22. DOI: 10.1186/s40657-015-0029-7
Citation:
Philip L. G. Birget, Stephen D. Larcombe. 2015: Maternal effects, malaria infections and the badge size of the house sparrow. Avian Research, 6(1): 22. DOI: 10.1186/s40657-015-0029-7
Philip L. G. Birget, Stephen D. Larcombe. 2015: Maternal effects, malaria infections and the badge size of the house sparrow. Avian Research, 6(1): 22. DOI: 10.1186/s40657-015-0029-7
Citation:
Philip L. G. Birget, Stephen D. Larcombe. 2015: Maternal effects, malaria infections and the badge size of the house sparrow. Avian Research, 6(1): 22. DOI: 10.1186/s40657-015-0029-7
The evolution of sexual signals is not only determined by immediate sexual selection but also by selection arising from the environment and the interaction with developmental effects. In this study we aimed to investigate how the badge size of male house sparrows (Passer domesticus) is correlated to avian malaria infections as well as to prenatal testosterone exposure, measured as the 2D:4D digit ratio. The rationale behind this study is that the immunosuppressive effect of maternal testosterone deposition combined with the fitness cost imposed by parasites may cause important trade-offs to the development of secondary sexual signals.
Methods
Assuming that vector abundance is a key variable associated with infection risk by avian malaria, we caught adult male sparrows from eight different populations in the Camargue, France, four of which were located in a vector-controlled area, and the other four in an untreated area. For each bird we measured its badge size, digit ratio and took blood to determine its infections status. We used PCR to identify the malaria parasite species and strain that caused the infection.
Results
Contrary to our expectation, prevalence of disease did not differ across the vector-treatment regions, with around 80 % of birds being infected in both areas, and those infections were caused largely by a single strain, Plasmodium relictum SGS1. Although infected birds had a badge size not significantly different from uninfected males, there was a condition-dependent association between badge size, infection status and maternal testosterone deposition.
Conclusions
This study illustrates that the complexity of temporal and ecological dimensions makes the relationships between disease, testosterone-related traits and secondary sexual signals that have been previously reported less general than thought.
Interactions between avian obligate brood parasites and
their hosts remain one of the most robust examples of
coevolutionary arms races (Davies, 2000;
Stoddard and Stevens, 2010; Kilner and Langmore, 2011). The best
studied and historically most prominent example of
such interactions is the evolved mimicry of host eggs
by parasites (Moksnes and Røskaft 1995; Cherry et al., 2007a; Moskát et al., 2008, 2010;
Spottiswoode and Stevens, 2010; Soler et al., 2012). Despite the extensive
similarities in the appearance of host and parasitic eggs
(Grim, 2005), many host species possess the ability
to discriminate between own and foreign eggs (Stoddard and Stevens, 2011). Much attention has recently
been given to the functional roles of light wavelengths
beyond the human perceptual range in avian egg discrimination, including the role of the shorter, ultraviolet
(UV) wavelengths (< 400 nm) (e.g. Honza et al., 2007), to which different species of birds within distantly related lineages are varyingly sensitive (e.g. Ödeen and
Håstad, 2003; Machovsky Capuska et al., 2011; Aidala
et al., 2012). For example, UV-reflectance is important
in recognizing and rejecting foreign eggs in the Blackcap (Sylvia atricapilla) (Honza and Polačiková, 2008)
and the Song Thrush (Turdus philomelos) (Honza et al., 2007). However, comparatively less emphasis has been
given to describing the visual sensitivities, UV or otherwise, of avian obligate brood parasites themselves.
Describing the visual sensitivities of specific bird species is vital, especially because the avian visual world
differs substantially from that of humans. For example, unlike trichromatic humans, who possess only three
classes of cone photoreceptor, birds possess five classes, four of which are directly responsible for color perception (Hunt et al., 2009). The short wavelength-sensitive
type 1 (SWS1) photoreceptor, which is responsible for
short-wavelength light detection, differs in its maximal
sensitivity depending on the amino acids present at
key 'spectral tuning' sites 86, 90, and 93 (following the
bovine Bos taurus rhodopsin numbering) (Wilkie et al., 2000; Yokoyama et al., 2000; Shi et al., 2001). Of these, amino acid residue 90 is particularly important for
mediating the degree of UV-sensitivity in avian species
(Wilkie et al., 2000; Hunt et al., 2009). Those species
possessing serine at site 90 (S90) are designated as having violet-sensitive (VS) pigments with a maximal sensitivity > 400 nm, and those possessing cysteine (C)90
are designated as having UV-sensitive (UVS) pigments
with a maximal sensitivity < 400 nm (Hart, 2001). Site
90 is also highly conserved, with S90 proposed to be
the ancestral state in all birds (Yokoyama and Shi, 2000;
Hunt et al., 2009), though recent analyses of basal paleognaths (which were not included in these earlier analyses) including extinct moa from New Zealand, predicted a uniform UVS SWS1 for all ratites and tinamou
allies (Aidala et al., 2012). Therefore, it is likely that C90
has (re-)evolved independently several times among
avian lineages (Hunt et al., 2009; Ödeen et al., 2010;
Machovsky Capuska et al., 2011; Ödeen et al., 2011, Aidala et al. 2012). Because microspectrophotometric
and genetic data are in accord with one another in avian
taxa for which both types of data are available (i.e. those
possessing S90 have VS SWS1 opsins and those possessing C90 have UVS SWS1 opsins), DNA sequencing of
the SWS1 opsin gene therefore permits accurate assessment of the degree of UV-sensitivity in any given avian
species (Ödeen and Håstad, 2003) before the need for
invasive and terminal physiological experimentation
to confirm the sequence-based predictions (Aidala and Hauber, 2010).
Much of the work on the functional role of UVreflectance and sensitivity in brood parasitic birds has
focused on explaining the lack of eggshell color-based
egg rejection to seemingly non-mimetic parasitic eggs.
Cherry and Bennett's (2001) UV-matching hypothesis
suggests that matching host/parasitic egg reflectance
along a UV-green opponency (which humans cannot
see) may explain the lack of rejection in acceptor host
species. Empirical support for this hypothesis, however, is equivocal. For example, blocking-the UV-reflectance
of Great-spotted Cuckoo (Clamator glandarius) eggs
does not affect rejection in Common Magpies (Pica
pica) (Avilés et al., 2006). However, the UVS/VS SWS1
sensitivity in this parasite-impacted host species has
not been described, although other Corvidae species
are predicted to be VS based on SWS1 DNA sequencing
(Ödeen and Håstad, 2003). More critically, no apparent
relationship between accepter/rejecter status and UVS/
VS SWS1 sensitivity appears to exist among hosts of the
North American generalist brood parasite, the Brownheaded Cowbird (Molothrus ater) and many of its hosts
(Underwood and Sealy, 2008; Aidala et al., 2012).
The degree of UV egg
color-matching/UV light sensitivity in New Zealand obligate brood parasite-host
systems is not yet described using reflectance spectrophotometric or avian perceptual
modeling data. The endemic Grey Warbler (Gerygone igata) is an ac-cepter
host of the local subspecies of the native Shin-ing Cuckoo (in Australia, called the Shining-bronze Cuckoo; Chalcites [Chrysococcyx] lucidus)
(McLean and Waas, 1987; also reviewed in Grim, 2006). In turn, the Whitehead (Mohoua
albicilla), Yellowhead (M. ochro-cephala), and Brown Creeper (M.
novaeseelandiae) are endemic hosts of the also endemic Long-tailed
Cuckoo (Urodynamis [Eudynamis] taitensis) (Payne, 2005). The Whitehead
and Yellowhead are both considered accept-er hosts (McLean and Waas, 1987;
Briskie, 2003), while the Brown Creeper ejects artificial Long-tailed Cuckoo
eggs at a rate of 67% (Briskie, 2003). DNA sequencing of the SWS1 photoreceptor
in the Grey Warbler and the Whitehead predicted a VS and a UVS SWS1 maximal
sensitivity, respectively (Aidala et al., 2012), whereas the predicted
sensitivities of their respective parasites are not well known.
Compared
to the large amount of effort spent char-acterizing the visual sensitivities of
host species, those of brood parasites themselves, especially to UV-wavelengths, have received considerably less attention. To
date, the SWS1 sensitivities have not been described in
any Cuculiformes species, although a study measuring
UV-reflectance in feather patches of 24 of 143 (17%)
total cuckoo species showed that 5 of the species (21%
of those measured) showed peaks in UV-reflectance
(Mullen and Pohland, 2008). As there are increasingly
more known inter-and intra-order variations in avian
UV-sensitivity (Ödeen and Håstad, 2003;
Machovsky Capuska et al., 2011; Aidala et al., 2012; Ödeen et al., 2012), and because visual systems among closely related
species may vary widely, and are likely to reflect speciesspecific sensory ecologies (Machovsky Capuska et al., 2012), reliance on species for which SWS1 sensitivity
data are available even within a lineage to approximate
the degree of UV-sensitivity may be inaccurate.
Characterization
of the UV-sensitivities of brood parasitic species is important for several
reasons. First, it will allow for stronger analysis of comparative per-ceptual
coevolution between hosts and parasites (An-derson et al., 2009). For example, recent egg color work using spectrophotometric measurements across the entire
avian visible range have provided new insights into the direction of
coevolutionary processes between hosts and parasites. Great Reed Warblers (Acrocephalus
arundinaceus) are more likely to reject mimetic Com-mon Cuckoo (Cuculus
canorus) eggs when this hosts?own eggs exhibit higher intraclutch
variation, a finding not in line with traditional predictions of
coevolution-ary theory, but validated by spectrophotometric mea-surements of
host eggs (Cherry et al., 2007a; see also Antonov et al., 2012). Similarly, Common Cuckoos may preferentially parasitize host nests with eggs more closely
resembling their own, also out of line with the theoretical assumption that
female cuckoos randomly choose local nests to parasitize (Cherry et al., 2007b). Second, describing the visual sensitivities of brood parasitic cuckoo
species will better inform studies ex-amining cuckoo-cuckoo competition
(Brooker et al., 1990) over host nesting sites using visual modeling analyses.
Third, it will allow for more accurate analysis of VS/UVS SWS1 opsin ancestral
states among avian species (Hunt et al., 2009; Aidala et al., 2012). Here, we
report the predicted maximal sensitivities of the SWS1 opsins in two New
Zealand native brood parasitic cuck-oos based on DNA sequencing of the SWS1 'pectral
tuning?region. In keeping with the general theoretical framework that host egg
rejection selects for egg color matching, and in turn, favors
UV-sensitivity in hosts, which in turn selects for UV-sensitivity in parasites, we expect the Shining Cuckoo that parasitizes the VS-pre-dicted Grey Warbler to
possess VS SWS1 opsins and the Long-tailed Cuckoo that parasitizes the
UVS-predicted Whitehead to possess UVS SWS1 opsins.
Methods
We collected ~100 μL blood samples that were stored
in Queen's lysis buffer from live Shining Cuckoos captured in mistnets during our field studies on avian hostparasite interactions (Anderson et al., 2009). We also
obtained tissue samples from frozen Long-tailed Cuckoos that died from migration-related window-collisions
and were stored in the Auckland Museum collection
(Gill and Hauber, 2012). Our collecting protocols were
approved by governmental and institutional animal research committees. Total genomic DNA was extracted
from tissue samples stored in ethanol using the DNeasy
Blood and Tissue Kit (Qiagen) according to manufacturer's instructions. DNA concentration (ng·μL–1) was
estimated using Nanodrop spectrophotometer.
Forward primers SU149a (Shining Cuckoo) or SU193
(Long-tailed Cuckoo) and reverse primer SU306b
(Ödeen and Håstad, 2003), modified to include M13-
tails, were used to sequence the SWS1 opsin gene. PCR
amplifications were carried out in 25 μL reaction volumes of 60 mmol·L–1 Tris-HCl ph 8.5, 15 mmol·L–1
(NH4)2SO4, 2.5 mmol·L–1 MgCl2, 0.3 mmol·L–1 of each
dNTP, 0.2 μmol·L–1 of each primer and 0.5 U of Platinum Taq polymerase (Invitrogen). Thermal cycling followed conditions outlined in Ödeen and Håstad (2003)
and was conducted in an ABI GeneAmp 9700 thermocycler.
An Exo/SAP treatment was used to purify PCR products: 5 μL PCR product was added to 0.2 μL of Exo I (GE
Healthcare), 0.1 μL Shrimp Alkaline Phosphatase (GE
Healthcare) and 1.7 μL UltraPure water (Invitrogen). We
incubated mixtures for 30 min at 37℃, then for 15 min
at 80℃ to ensure enzyme inactivation. A BigDye Terminator Cycle Sequencing kit v3.1 (Applied Biosystems)
was used to sequence samples in both directions with
M13 forward and reverse primers. Each sequencing reaction consisted of 1 μL BigDye Terminator Mix, 3.5 μL
5× sequencing buffer, 0.2 μmol·L–1 primer, 1 μL DMSO
and 2 μL PCR product. Agencourt CleanSeq (Beckman
Coulter) was used according to manufacturer's instructions to purify sequencing reactions and analyzed using an ABI 3100 automated sequencer. Chromas Pro (Technelysium Pty. Ltd.) was used to edit sequences following
which they were exported to BioEdit (Hall, 1999) for
alignment and translation.
Results
The two Shining Cuckoo samples generated a sequence
length of 119 base pairs (bp) each. The two Long-tailed
Cuckoo samples generated a sequence length of 74 bp
each. All sequences have been made available on GenBank (Accession numbers HM159121–HM159124).
We detected no intraspecific or intrafamilial variation
in either the gene or amino acid sequences, except for
the codons at residue 95; however, both of these code
for the amino acid phenylalanine (Table 1). We found
only two ambiguities in one Long-tailed Cuckoo sample, whereas the other Long-tailed Cuckoo possessed
the same codons and amino acid residues as the two
Shining Cuckoo samples (Table 1). After alignment, all
samples possessed S86, S90, and T93, which predict VS
for both of these cuckoo species' SWS1 opsin photoreceptors.
Table
1.
Predicted VS/UVS SWS1 opsin state of two New Zealand cuckoo species based on SWS1 amino acid sequences. Passerine
host species are shown below each cuckoo species and were adapted from Aidala et al. (2012). Spectral tuning sites 86, 90, and 93 are
underlined.
This is the first study to report on the sequence of SWS1
receptors and to predict short-wavelength visual sensitivities of New Zealand's brood parasitic native Shining
Cuckoos and endemic Long-tailed Cuckoos. Substituting S for A at amino acid residue 86 (A86S substitution)
produces a short-wave shift of 1 nm, a T93V substitution produces a long-wave shift of 3 nm, and a C90S
substitution produces a 35 nm long-wave shift in the
UVS SWS1 opsin of the Budgerigar (Melopsittacus undulatus) (Wilkie et al. 2000). The same C90S substitution in the Zebra Finch (Taeniopygia guttata) produces
a similar-magnitude long-wave shift of SWS1 maximal
sensitivity from 359 to 397 nm (Yokoyama et al., 2000).
Thus, despite possessing S86 and T93 in both species, the presence of S90 predicts that the SWS1 maximal
sensitivities of our cuckoo samples should be well within the visible-violet portion of the light spectrum, or VS
(Table 1).
This finding is contradictory to our original prediction that only the Long-tailed Cuckoo should possess
UVS SWS1 opsins due to the predicted UVS SWS1 of
its Whitehead host (in contrast with the VS SWS1 of
the Shining Cuckoo's Grey Warbler host; Table 1). Accordingly, we did not observe a distinct pattern between
predicted SWS1 sensitivities of our cuckoo samples and
those of their hosts. Both the Grey Warbler and Whitehead are non-ejector hosts of the Shining and Longtailed Cuckoos respectively, yet these host species differ
in their predicted SWS1 maximal sensitivities; DNA
sequencing of the SWS1 photoreceptor gene predicted
a VS SWS1 in the Grey Warbler but a UVS SWS1 in the
Whitehead (Aidala et al., 2012). Predicted sensitivities of the other two Long-tailed Cuckoo hosts, the
non-ejector Yellowhead, and the artificial egg-ejecting
Brown Creeper are not yet described from molecular
sequencing data. Also undocumented is the degree of
physical or perceptual host-parasite egg color matching, in the UV-portion specifically, and in the avianvisible spectrum overall, in these two host-parasite systems. Nonetheless, human-visible assessment suggests some level of mimicry between Long-tailed Cuckoos
and their hosts (Briskie, 2003), whereas the dark Shining
Cuckoo's eggs may be cryptic, and not mimetic, in the
enclosed nests of the Grey Warbler hosts (see Langmore
et al., 2009).
An alternative to perceptual coevolutionary processes mediating the detection of parasitic eggs in New
Zealand hosts is that the cost of accepting parasitic eggs
might be offset by recognizing and rejecting parasitic
cuckoo chicks (Davies, 2000). Despite a lack of direct
behavioral or sensory data in our focal systems, there is
evidence of parasitic chick detection and ejection based
on visual appearance in the closely related Australian
Large-billed Gerygone (Gerygone manirostris)/Little
Bronze-cuckoo (Chalcites [Chrysococcyx] minutillus)
(Sato et al., 2010) and Superb Fairy-wren (Malurus cyaneus)/Shining Cuckoo host-parasite systems (Langmore
et al., 2003; see also Langmore et al., 2011). Further, there is evidence of evolved call-matching of the begging calls of Grey Warblers by Shining Cuckoo chicks
based on both sound recordings (McLean and Waas, 1987) and comparative phylogenetic inference (Anderson et al., 2009). Similarly, McLean and Waas (1987)
noted and Ranjard et al. (2010) provided bioacoustic
evidence for the evolved similarity between the begging
calls of the Long-tailed Cuckoo and its Mohoua spp.
hosts. Other parasitic cuckoo-host systems, including
the Horsefield's Bronze-cuckoo (Chalcites [Chrysococcyx] basalis) and its Superb Fairy-wren (Malurus cyaneus) hosts (Langmore et al., 2003, 2008; Colombelli-Negrel et al., 2012), the Diederick Cuckoo (Chrysococcyx
caprius) and its hosts, and the Koel (Eudynamis scolopacea) and its House Crow (Corvus splendens) hosts have
also been shown to have similar begging calls (reviewed
in Grim, 2006).
Characterizing the visual sensitivities of diverse avian
lineages, including parasitic cuckoo species, is an important step in understanding the coevolution of visual
perception/parasitic egg rejection behaviors in hostparasite interactions and sensory ecology. These studies
form the basis for future visual modeling and sensoryphysiological studies for more accurate description of
the perceptual systems of focal cuckoo species. Future
studies should investigate the behavioral significance
of egg color matching in driving sensory coevolution
using appropriate visual perceptual modeling analyses
of both host and parasitic species (Aidala and Hauber, 2010). Additional Cuculiformes species should also be
included in future analyses in order to better describe
the degree of V/UV-matching in host-parasite egg color
mimicry and its perception and the ecological variables
that may drive or hinder the evolution of UV-sensitivity
amongst parasitic and non-parasitic cuckoos (Krüger et al., 2009).
Acknowledgments
All field work was conducted in accordance
with local animal ethics rules and regulations in New Zealand
and the University of Auckland. We thank Brian Gill for
providing tissue samples of Long-tailed Cuckoos at the Auckland
Museum and Andrew Fidler for advice on sequencing. We also
thank the many volunteers for assistance in field work, and
two anonymous reviewers for the helpful comments on our
manuscript. This research was funded by the US National Science
Foundation and the Graduate Center of the City University of
New York (to ZA and to MEH), a Foundation for Research, Science, and Technology postdoctoral fellowship (to MGA), and
the National Geographic Society, the PSC-CUNY grant scheme, and the Human Frontier Science Program (to MEH).
Anderson TR. Biology of the ubiquitous house sparrow: from genes to populations. New York: Oxford University Press; 2006.
Andersson MB. Sexual selection. Princeton: Princeton University Press; 1994.
Badyaev AV, Uller T. Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc B. 2009;364(1520):1169-77.
Biard C, Saulnier N, Gaillard M, Moreau J. Carotenoid-based bill colour is an integrative signal of multiple parasite infection in blackbird. Naturwissenschaften. 2010;97(11):987-95.
Bichet C, Scheifler R, Coeurdassier M, Julliard R, Sorci G, Loiseau C. Urbanization, trace metal pollution, and malaria prevalence in the house sparrow. PLoS One. 2013;8(1):53866.
Bichet C, Sorci G, Robert A, Julliard R, Lendvai AZ, Chastel O, Garnier S, Loiseau C. Epidemiology of Plasmodium relictum infection in the house sparrow. J Parasitol. 2014;100(1):59-65.
Bonneaud C, Pérez-Tris J, Federici P, Chastel O, Sorci G. Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution. 2006;60(2):383-9.
Buchanan K, Evans M, Goldsmith A. Testosterone, dominance signalling and immunosuppression in the house sparrow, Passer domesticus. Behav Ecol Sociobiol. 2003;55(1):50-9.
Buchanan K, Evans M, Roberts M, Rowe L, Goldsmith A. Does testosterone determine dominance in the house sparrow, Passer domesticus? an experimental test. J Avian Biol. 2010;41(4):445-51.
Burley NT, Foster VS. Digit ratio varies with sex, egg order and strength of mate preference in zebra finches. Proc R Soc Lond Ser B. 2004;271(1536):239-44.
Cain KE, Burns CMB, Ketterson ED. Testosterone production, sexually dimorphic morphology, and digit ratio in the dark-eyed junco. Behav Ecol. 2013;24(2):462-9.
Cornet S, Nicot A, Rivero A, Gandon S. Evolution of plastic transmission strategies in avian malaria. PLoS Pathog. 2014;10(9):1004308.
Cornwallis CK, Uller T. Towards an evolutionary ecology of sexual traits. Trends Ecol Evol. 2010;25(3):145-52.
Crawley MJ. The R Book. Chichester: Wiley; 2007.
Danchin É, Charmantier A, Champagne FA, Mesoudi A, Pujol B, Blanchet S. Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat Rev Genet. 2011;12(7):475-86.
Dolnik OV, Hoi H. Honest signalling, dominance hierarchies and body condition in house sparrows Passer domesticus (Aves: Passeriformes) during acute coccidiosis. Biol J Linn Soc. 2010;99(4):718-26.
Duffy DL, Bentley GE, Drazen DL, Ball GF. Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European Starlings. Behav Ecol. 2000;11(6):654-62.
Folstad I, Karter AJ. Parasites, bright males, and the immunocompetence handicap. Am Nat. 1992;139(3):603-22.
Galván I, Alonso-Alvarez C. Yolk testosterone shapes the expression of a melanin-based signal in great tits: an antioxidant-mediated mechanism? J Exp Biol. 2010;213(18): 3127-30.
Garamszegi LZ, Møller AP. The interspecific relationship between prevalence of blood parasites and sexual traits in birds when considering recent methodological advancements. Behav Ecol Sociobiol. 2012;66(1):107-19.
Gonzalez G, Sorci G, Smith LC, Lope F. Testosterone and sexual signalling in male house sparrows (Passer domesticus). Behav Ecol Sociobiol. 2001;50(6):557-62.
Griffith SC. A trade-off between reproduction and a condition-dependent sexually selected ornament in the house sparrow Passer domesticus. Proc R Soc Lond B. 2000;267(1448):1115-9.
Griffith SC, Owens IP, Burke T. Environmental determination of a sexually selected trait. Nature. 1999;400(6742):358-60.
Groothuis TG, Eising CM, Dijkstra C, Müller W. Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett. 2005;1(1):78-81.
Hamilton WD, Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982;218(4570): 384-7.
Jensen H, Svorkmo-Lundberg T, Harald Ringsby T, Sæther BE. Environmental influence and cohort effects in a sexual ornament in the house sparrow, Passer domesticus. Oikos. 2006;114(2):212-24.
Knowles SC, Wood MJ, Alves R, Wilkin TA, Bensch S, Sheldon BC. Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Mol Ecol. 2011;20(5):1062-76.
Labbé P, Lenormand T, Raymond M. On the worldwide spread of an insecticide resistance gene: a role for local selection. J Evol Biol. 2005;18(6):1471-84.
Laucht S, Dale J. Development of badges of status in captive male house sparrows (Passer domesticus) in relation to the relative ornamentation of flock-mates. Ethology. 2012;118(7):644-53.
Laucht S, Dale J, Mutzel A, Kempenaers B. Individual variation in plasma testosterone levels and its relation to badge size in house sparrows, Passer domesticus: It's a night-and-day difference. Gen Comp Endocrinol. 2011;170(3):501-8.
Lenormand T, Bourguet D, Guillemaud T, Raymond M. Tracking the evolution of insecticide resistance in the mosquito Culex pipiens. Nature. 1999;400(6747):861-4.
Liker A, Barta Z. Male badge size predicts dominance against females in house sparrows. Condor. 2001;103(1):151.
Loiseau C, Richard M, Garnier S, Chastel O, Julliard R, Zoorob R, Sorci G. Diversifying selection on mhc class i in the house sparrow (Passer domesticus). Mol Ecol. 2009;18(7):1331-40.
Loiseau C, Zoorob R, Robert A, Chastel O, Julliard R, Sorci G. Plasmodium relictum infection and mhc diversity in the house sparrow (Passer domesticus). Proc R Soc B. 2011;278(1709):1264-72.
Mackinnon M, Marsh K. The selection landscape of malaria parasites. Science. 2010;328(5980):866-71.
Manning JT. Digit ratio: a pointer to fertility, behavior, and health. New Jersey: Rutgers University Press; 2002.
Marzal A, Ricklefs RE, Valkiunas G, Albayrak T, Arriero E, Bonneaud C, Czirjak GA, Ewen J, Hellgren O, Dita H, et al. Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS One. 2011;6(7):21905.
Mazuc J, Bonneaud C, Chastel O, Sorci G. Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett. 2003;6(12):1084-90.
Moreno-Rueda G. Experimental test of a trade-off between moult and immune response in house sparrows Passer domesticus. J Evol Biol. 2010;23(10):2229-37.
Møller AP. Social control of deception among status signalling house sparrows. Passer domesticus. Behav Ecol Sociobiol. 1987;20(5):307-11.
Møller A, Erritzøe J. Acquisition of breeding coloration depends on badge size in male house sparrows Passer domesticus. Behav Ecol Sociobiol. 1992;31(4):271-7.
Müller W, Lessels CM, Korsten P, von Engelhardt N. Manipulative signals in family conflict? On the function of maternal yolk hormones in birds. Am Nat. 2007;169:84-96.
Nakagawa S, Ockendon N, Gillespie DO, Hatchwell BJ, Burke T. Assessing the function of house sparrows' bib size using a flexible meta-analysis method. Behav Ecol. 2007;18(5):831-40.
Navarro C, De Lope F, Marzal A, Møller A. Predation risk, host immune response, and parasitism. Behav Ecol. 2004;15(4):629-35.
Navarro C, de Lope F, Møller AP. Digit ratios (2d: 4d), secondary sexual characters and cell-mediated immunity in house sparrows. Passer domesticus. Behav Ecol Sociobiol. 2007;61(8):1161-8.
Partecke J, Schwabl H. Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Dev Neurobiol. 2008;68(14):1538-48.
Poiani A, Goldsmith A, Evans M. Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model. Behav Ecol Sociobiol. 2000;47(4):230-42.
Ponçon N, Toty C, L'ambert G, Le Goff G, Brengues C, Schaffner F, Fontenille D. Population dynamics of pest mosquitoes and potential malaria and West Nile virus vectors in relation to climatic factors and human activities in the Camargue, France. Med Vet Entomol. 2007;21(4):350-7.
Poulin B. Indirect effects of bioinsecticides on the nontarget fauna: the Camargue experiment calls for future research. Acta Oecol. 2012;44:28-32.
Randolph SE, Rogers DJ. The arrival, establishment and spread of exotic diseases: patterns and predictions. Nat Rev Microbiol. 2010;8(5):361-71.
Roberts ML, Buchanan KL, Evans MR. Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav. 2004;68(2):227-39.
Roberts ML, Buchanan KL, Goldsmith AR, Evans MR. The role of testosterone in bib size determination in the male house sparrow Passer domesticus, is age dependent. J Avian Biol. 2012;43(3):264-72.
Ross R. The prevention of malaria. London: John Murray; 1910.
Saino N, Møller A, Bolzerna A. Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behav Ecol. 1995;6(4):397-404.
Sandell MI, Tobler M, Hasselquist D. Yolk androgens and the development of avian immunity: an experiment in jackdaws (Corvus monedula). J Exp Biol. 2009;212(6):815-22.
Schwabl H. Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci. 1993;90(24):11446-50.
Schwabl H. Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol Part A. 1996;114(3):271-6.
Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996;11(8):317-21.
Stearns S. The Evolution of Life Histories. Oxford: OUP; 1992.
Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H. Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J Anim Ecol. 2005;74(4):675-82.
Valkiunas G. Avian malaria parasites and other haemosporidia. Boca Raton: CRC Press; 2004.
Veiga JP, Puerta M. Nutritional constraints determine the expression of a sexual trait in the house sparrow, Passer domesticus. Proc R Soc Lond Ser B. 1996;263(1367):229-34.
Verhulst S, Dieleman S, Parmentier H. A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proc Natl Acad Sci. 1999;96(8):4478-81.
Waldenström J, Bensch S, Hasselquist D, Östman Ö. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol. 2004;90(1):191-4.
Wood MJ, Cosgrove CL, Wilkin TA, Knowles SC, Day KP, Sheldon BC. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol Ecol. 2007;16(15):3263-73.
Zahavi A. Mate selection-a selection for a handicap. J Theor Biol. 1975;53(1):205-14.
Zuk M. Sex differences in parasite infections: patterns and processes. Int J Parasitol. 1996;26(10):1009-23.
Table
1.
Predicted VS/UVS SWS1 opsin state of two New Zealand cuckoo species based on SWS1 amino acid sequences. Passerine
host species are shown below each cuckoo species and were adapted from Aidala et al. (2012). Spectral tuning sites 86, 90, and 93 are
underlined.
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