Behavioral Ecology Vol. 11 No. 3: 345-349
© 2000 International Society for Behavioral Ecology
Forum |
A novel evolutionary pattern of reversed sexual dimorphism in fairy wrens: implications for sexual selection
Department of Ecology and Evolution, University of Chicago, 1101 East 57th Street, Chicago, IL 60637, USA
Address correspondence to J. P. Swaddle at the Centre for Behavioural Biology, School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK. E-mail: john{at}swaddle.com .
Received 23 December 1998; revised 9 June 1999; accepted 26 September 1999.
Reversed sexual dimorphism (females being larger than males) occurs in
several bird groups, including hawks and vultures (Accipitridae), falcons
(Falconidae), sandpipers and snipe (Scolopacidae), phalaropes (Charadriidae),
jacanas (Jacanidae), skuas (Stercorariidae), boobies (Sulidae), frigate birds
(Fregatidae), owls (Strigiformes), cuckoos (Cuculidae), hummingbirds
(Trochilidae), manakins (Pipridae), and some ratites (Struthioniformes). In
most cases, reversed sexual dimorphism (RSD) is present in many traits, and
hence selection has been presumed to act non-independently on several
characters (Lande and Arnold,
1983
). Hence, RSD has commonly been discussed in terms of
differences in body size (Mueller,
1990). In this study, we report a novel pattern of RSD in fairy
wrens (Maluridae), which has important evolutionary implications for the ways
in which sexual dimorphism can occur and the mechanisms of sexual
selection.
We examined patterns of morphological sexual dimorphism, based on published
data (Rowley and Russell,
1997; Schodde,
1982) and our own measurements (described later), within a
molecular phylogeny for the Maluridae
(Christidis and Schodde, 1997).
This analysis revealed at least two independent occurrences of RSD in tail
length (Figure 1). In one of
these cases, the orange-crowned fairy wren Clytomyias insignis, the
reversed dimorphism is associated with a small relative increase in tarsus and
wing length in the female, as is commonly observed in species with RSD.
However, reversed tail dimorphism in red-backed, white-shouldered and
white-winged fairy wrens (M. melanocephalus, M. alboscapulatus, and
Malurus leucopterus, respectively) is not associated with an increase
in size of other female traits (Table
1). In the first two species, the male is larger in terms of
tarsus and wing length, but the female has a significantly longer tail. Two
island subspecies of the third species (M. l. leucopterus and M.
l. edouardi) show the same pattern, but the mainland subspecies (which we
have used as the designate species for the phylogeny) appears monomorphic in
terms of tail length (M. l. leuconotus;
Table 1). Although tail-length
differences have previously been noted for fairy wren species
(Schodde, 1982), the
classification of RSD has not been formally described or quantitatively
studied in any of these species. As far as we are aware, the RSD of a single
trait (in an opposite direction to the body size dimorphism) is a novel
pattern of evolution of tail elongation in birds. In a survey of published
incidences of RSD, we could not find a single account that matched the
morphological patterns observed in this cluster of three species of fairy
wrens.
|
|
To explore whether this pattern of RSD in fairy wrens has arisen due to
tail elongation in the female or tail shortening in the male, we examined
changes in tail length, tarsus length, and wing length using the reduced
squared-change parsimony algorithm in MacClade
(Maddison and Maddison, 1992).
In particular, we focused on the nodes preceding and including those of the
Malurus RSD complex (indicated as nodes 1 to 4 in
Figure 1) to reconstruct the
ancestral morphological states. Both tarsus and wing length (commonly
interpreted as indicators of body size) decrease through the complex, with
males remaining larger than females (Figure
2a, b). Changes in tail length show a very different pattern
(Figure 2c). Initially (i.e.,
at node 1), males possess longer tails than females; but male tail length
decreases at a faster rate than females, resulting in relatively longer tails
in the females (nodes 1 to 3). When M. alboscapulatus branches off at
node 3, tail length is further reduced, and the RSD is increased due to a
larger reduction in tail length in the male. A slightly different pattern is
observed as M. melanocephalus and M. leucopterus diverge at
node 4. Male tail length is reduced further in M. melanocephalus and
female tails are reduced only slightly (resulting in a large RSD), whereas
overall tail length increases in M. leucopterus. The increase in tail
length in M. leucopterus is shown to a greater extent in the males,
resulting in sexual monomorphism (although two subspecies of M.
leucopterus appear to regain tail length RSD).
|
Most hypotheses for the evolution of RSD have stressed the importance of
sexual selection acting on increased female size
(Mueller, 1990;
Olsen and Cockburn, 1993) and
simultaneous decreased male size (Amadon,
1975; Jehl and Murray,
1986; Lande, 1980;
Mueller, 1990). We cannot
invoke such hypotheses here, as there is no associated increase in female size
in the species exhibiting RSD. Therefore, we need to consider alternative
mechanisms by which the pattern of RSD could have arisen in these fairy wrens.
There are no apparent systematic differences in mating system that could
explain the differences in tail dimorphism across the species
(Björklund,
1990; Schodde,
1982). Similarly, ecological specialization of these species
appears to postdate the evolutionary trend for decreased male tail length
(Schodde, 1982) and so cannot
explain the observed dimorphism. The RSD species are also so obviously
sexually dichromatic that it seems unlikely the tail length dimorphism could
have evolved to reduce competition between mated pairs (or the sexes) for
access to ecological resources such as food
(Shine, 1989). We can also
exclude hypotheses for RSD based on female ornamentation
(Amundsen et al., 1997), as it
appears that male tail length is decreasing rather than female tail length
increasing.
We have generated three nonmutually exclusive hypotheses that could explain
the observed pattern of RSD in fairy wrens. First, decreased male tail length
could be a sexually selected ornament and could be used as a signaling device
to discriminate among males (Jehl and
Murray, 1986). Two of the species exhibiting RSD are known to
exhibit unusually high levels of sexual promiscuity (approximately 50% of
young are the result of an extrapair copulation in M. melanocephalus;
Karubian J, unpublished data), allowing for high variance in male reproductive
success and the opportunity for intense sexual selection
(Webster et al., 1995). In
each species, birds hold their tail in a cocked, upright position, which has
led Schodde (1982) to describe
the tail of fairy wrens as reflecting social position and displays involving
the tail as being central to fairy wren social organization. Hence, it is
possible that the morphology of the tail (in association with its movement)
may be an important sexual signaling device. To test this hypothesis, one
could perform mate choice and social dominance trials in which the length of
males' tails is manipulated independent of other morphological and behavioral
characters.
Our second hypothesis predicts that decreased male tail length could render
a mechanical advantage. These species of fairy wren possess graduated tails,
which are thought to be aerodynamically costly ornaments when elongated
(Thomas, 1993). Therefore,
reduction of tail length could lead to increased flight performance and hence
reduced predation risk, increased foraging efficiency, or lower flight costs
for interterritory forays to seek extrapair copulations. The reduction in wing
length observed across the clade (Figure
2b) may further increase flight costs and hence be an additional
factor driving the reduction of tail elongation
(Balmford et al., 1994). For
this hypothesis to account for RSD, there would have to be differential flight
costs associated with male and female behaviors and/or some partitioning of
roles between the sexes in terms of flight behaviors
(Lundberg, 1986). The
influence of tail morphology on flight could be tested directly by tail length
manipulations and controlled flight observations which include quantification
of aerodynamic and biomechanical parameters to assess the flight costs of
decreasing tail length (cf. Swaddle et
al., 1999).
Finally, males and females may be subject to the same (directional)
selection pressures acting on tail length, but the males have responded to a
greater degree than females. This could occur if there was greater genetic
variation in tail length in males but similar genetic variation in tarsus and
wing length between the sexes (Shine,
1988). Genetic variation for the various morphological characters
could be assessed by heritability studies.
To confirm the pattern of RSD in fairy wrens and to examine the
plausibility of our hypotheses, we analyzed sex, age, morphological, breeding,
and behavioral data from an on-going field study of red-backed fairy wrens
M. m. melanocephalus in Queensland (Karubian J, unpublished data).
M. melanocephalus live in stable, socially monogamous pairs which are
often accompanied by helpers (male offspring which delay dispersal from their
natal territory to assist their parents with subsequent reproductive efforts).
Helper males retain dull, femalelike plumage until they obtain their own
breeding territory, which usually occurs by 2 years of age
(Rowley and Russell, 1997;
Karubian J, unpublished data).
Our analysis of among-individual morphological data from M. melanocephalus revealed significant sexual dimorphism in adult (>1 year old) wing length, tarsus length, and body mass; males are larger and heavier than females (male wing length = 40.93 ± 0.96 mm, N = 50, female wing length = 40.47 ± 1.01 mm, N = 39, t87 = 2.18, p =.032; male tarsus length = 20.97 ± 0.81 mm, N = 37, female tarsus = 20.36 ± 0.91 mm, N = 23, t42 = 2.63, p = 0.012; male mass = 7.71 ± 0.67 g, N = 51, female mass = 7.05 ± 0.97 g, N = 35, t84 = 3.70, p <.001). However, adult male red-backed fairy wrens have significantly shorter tails than females during the breeding season (male breeding tail length = 47.28 ± 4.31 mm, N = 37, female breeding tail length = 52.25 ± 6.66 mm, N = 31, t66 = 3.71, p <.001) but not during the nonbreeding season (male nonbreeding tail length = 57.90 ± 5.87 mm, N = 10, female nonbreeding tail length = 55.92 ± 2.82 mm, N = 6, t14 = 0.77, p =.46). In addition, tail lengths of adult males that are socially dominant in a group (and older; Karubian J, unpublished data) are significantly shorter than tail lengths of subordinate males (tail length for breeding males = 47.38 ± 4.32 mm, N = 44; tail length for helpers = 52.26 ± 2.94 mm, N = 4; t46 = 2.20, p =.033).
Morphology is known to vary with age and social status, as well as sex, in
many species of fairy wrens (Schodde,
1982). Therefore, to minimize the influence of age and social
status on sexual dimorphism, we also analyzed within-individual changes in
tail length and wing length between the nonbreeding and breeding season for
adult males (N = 11) and females (N = 9) (tarsus length does
not alter seasonally, but males possessed longer tarsi than females;
t18 = 3.13, p =.008). These data corroborate the
among-individual sample. Males had longer wings in both the breeding
(t18 = 4.39, p <.001) and nonbreeding season
(t18 = 2.95, p =.009). Males possessed shorter
tails than females in the breeding season, but there was no sexual dimorphism
in tail length during the non-breeding season
(Figure 3).
|
Hence, RSD in tail length is found only in the breeding season. This is
consistent with our hypothesis 1 (sexual selection), but inconsistent with
hypothesis 3 (similar selection on males and females). For hypothesis 2
(flight energetics) to be valid, flight demands must be higher in males than
in females in the breeding season but not at other times of the year. Most
empirical data suggest that flight demands are higher for breeding females, as
they experience the increased physiological and energetic demands of egg
production and flying while gravid (Carey,
1996). However, breeding male red-backed fairy wrens often make
long flights (>400 m) between breeding territories, whereas females and
secondary males do not. In 500 focal samples conducted during the 1997-1998
breeding season, males in nonbreeding plumage and females were never observed
to leave their territory. Males in bright plumage, however, left the territory
an average of 0.4 times per 30-min observation period to intrude upon other
breeding territories (Karubian J, unpublished data). Males presumably make
such forays in search of extrapair mates. As fairy wrens are notoriously poor
fliers and rarely fly for extended periods of time (most of their locomotion
involves hopping or taking short flights between foraging sites;
Schodde, 1982), these
observations indicate that biomechanical considerations could explain the
reduction in male tail length during the breeding season. It will be important
to directly quantify the flight costs of different tail morphologies in these
and closely related species.
Whichever mechanism accounts for the RSD in tail length of this group of
fairy wrens, this novel evolutionary pattern has implications for evolutionary
theory. The reported pattern suggests that reduced trait size can be the
selected ornamental trait in birds. We are aware that this pattern of male
tail shortening also occurs in Cisticolas (Lewis M, unpublished data),
although there are as yet no published reports. All other reported incidences
of sexual dimorphism in tail length have presumed tail elongation in one sex
(most commonly the male; Andersson,
1994). This is clearly not the case in fairy wrens, and hence
other reports of tail elongation should be evaluated within a phylogenetic
framework to indicate the magnitude and direction of changes in tail length.
Without a phylogenetic approach we could have equally assumed that female tail
length was increasing and hypothesized that females were the ornamented sex.
In addition, current accepted wisdom proposes that increased ornament size
increases trait costs and enforces honesty upon trait design
(Zahavi, 1975). If tail length
differences are used as a signal in fairy wrens, this system would provide a
fascinating test (and potential contradiction) of the handicap theory.
Although the functional importance of the fairy wren tail is not yet clear,
our data support the notion that the shortened male tail is advantageous
during the breeding season and that there is selection for decreased male tail
length in these species. The pattern of RSD in this fairy wren complex is also
novel in that it provides evidence that sexually dimorphic selection pressures
can act in the opposite direction in body size (tarsus and wing length) and
tail length within a species. Most evolutionary explanations of sexual
dimorphism have assumed that directional selection acting on the size of one
trait will tend to drag along other traits through genetic correlations
(Lande, 1980;
Lande and Arnold, 1983).
Tarsus and wing length are good indicators of body size in birds; hence
selection appears to be acting in opposite directions (relative to females)
for male body size and male tail length. Therefore, our findings indicate that
current models for the evolution of sexual dimorphism are not comprehensive
and that tail length RSD in the fairy wrens can provide a novel system in
which to test sexual selection theory.
ACKNOWLEDGEMENTS
We thank A. Cockburn, M. Lewis, K. Tarvin, and D. Schodde for assistance and discussion. J.P.S. was funded by a Royal Society of London University Research Fellowship. S.P.-J. was financially supported by the National Science Foundation (grant IBN-9724053) and the Wettenhall Foundation. Field work of J.K. was supported by the American Museum of Natural History, American Ornithologist's Union, and the Hinds Fund of the University of Chicago.
REFERENCES
Amadon D, 1975. Why are female birds larger than males? Raptor Res 9: 1-11.
Amundsen T, Forsgren E, Hansen LTT, 1997. On the
function of female ornaments: male bluethroats prefer colourful males.
Proc R Soc Lond B 264:
1579-1586.
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Balmford A, Jones IL, Thomas ALR, 1994. How to compensate for costly sexually selected tail: the origin of sexually dimorphic wings in long-tailed birds. Evolution 48: 1062-1070.[Web of Science]
Björklund M, 1990. A phylogenetic interpretation of sexual dimorphism in body size and ornament in relation to mating system in birds. J Evol Biol 3: 171-183.[Web of Science]
Carey C, 1996. Female reproductive energetics. In: Avian energetics and nutritional ecology (Carey C, ed). New York: Chapman and Hall; 324-474.
Christidis L, Schodde R, 1997. Relationships within the Australo-Papuan fairy-wrens (Aves: Maluridae): an evaluation of the utility of allozyme data. Aust J Zool 45: 113-119.
Jehl JR Jr, Murray BG Jr, 1986. The evolution of normal and reverse sexual size dimorphism in shorebirds and other birds. Curr Ornithol 3: 1-86.
Lande R, 1980. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34: 292-305.[Web of Science]
Lande R, Arnold S, 1983. The measurement of selection on correlated characters. Evolution 37: 1210-1226.[Web of Science]
Lundberg A, 1986. Adaptive advantages of reversed sexual size dimorphism in European owls. Ornis Scand 17: 133-140.
Maddison WP, Maddison DR, 1992. MacClade: analysis of phylogeny and character evolution. Sunderland, Massachusetts: Sinauer Associates.
Mueller HC, 1990. The evolution of reversed sexual dimorphism in size in monogamous species of birds. Biol Rev 65: 553-585.[Web of Science]
Olsen PD, Cockburn A, 1993. Do large females lay small eggs? Sexual dimorphism and the allometry of egg and clutch volume. Oikos 66: 447-453.[Web of Science]
Rowley I, Russell E, 1997. Fairy-wrens and grasswrens. Oxford: Oxford University Press.
Schodde R, 1982. The fairy-wrens. Melbourne: Lansdowne Editions.
Shine R, 1988. The evolution of large body size in females: a critique of Darwin's "fecundity advantage" model. Am Nat 131: 124-131.[Web of Science]
Shine R, 1989. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64: 419-461.[Medline]
Swaddle JP, Williams EV, Rayner JMV, 1999. The effect of simulated flight feather moult on escape take-off performance in starlings. J Avian Biol 30: 351-358.
Thomas ALR, 1993. On the aerodynamics of birds' tails. Phil Trans R Soc Lond B 340: 361-380.
Webster MS, Pruett-Jones S, Westneat D, Arnold S, 1995. Measuring the effects of pairing success, extra-pair copulations and mate quality on the opportunity for sexual selection. Evolution 49: 1147-1157.[Web of Science]
Zahavi A, 1975. Mate selection: a selection for a handicap. J Theor Biol 53: 205-214.[Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||