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Convergent evolution in mechanical design of lamnid sharks and tunas

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the experimental pressure range. If oxygen solubility does increase 26. Gessmann, C. K. & Rubie, D. C. The origin of the depletions of V, Cr, and Mn in the mantles of the
Earth and Moon. Earth Planet. Sci. Inter. 184, 95–107 (2000).
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ocean depth required on the Earth to satisfy the FeO content of the silicate and iron-rich metal liquids: a diamond-anvil cell study. Earth Planet. Sci. Inter. 209, 245–255
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increasing pressure, the solubility of oxygen in Fe-alloy is predicted Supplementary Information accompanies the paper on www.nature.com/nature.
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Acknowledgements We thank H. Fischer, G. Herrmannsdörfer, D. Krausse and H. Schulze for
three possibilities for the fate of the dissolved oxygen, all of which technical assistance. The German Science Foundation (DFG) supported this research.
could be important. (1) FeO precipitated from liquid metal between
the base of the magma ocean and the proto-core, thus creating Competing interests statement The authors declare that they have no competing financial
chemical heterogeneities that may still exist in the lowermost interests.
mantle8. (2) Oxygen was transported by liquid metal to the core,
where FeO precipitated to form the D 00 layer at the core–mantle Correspondence and requests for materials should be addressed to D.C.R.
([email protected]).
boundary9. (3) At least part of the oxygen may still be dissolved in
the core (up to 8 wt% according to our model), thus contributing
significantly to its light-element budget10,11. If oxygen does become
more soluble in liquid metal at pressures higher than our experi-
mental conditions, then that would tend to favour this final
possibility. In contrast, the martian core is unlikely to contain any ..............................................................
dissolved oxygen, which is consistent with its probable high sulphur
content7. A Convergent evolution in mechanical
Received 6 October 2003; accepted 8 March 2004; doi:10.1038/nature02473. design of lamnid sharks and tunas
1. Li, J. & Agee, C. B. Geochemistry of mantle–core differentiation at high pressure. Nature 381, 686–689
(1996). Jeanine M. Donley1, Chugey A. Sepulveda1, Peter Konstantinidis2,
2. Li, J. & Agee, C. B. The effect of pressure, temperature, oxygen fugacity and composition on
partitioning of nickel and cobalt between liquid Fe-Ni-S alloy and liquid silicate: Implications for the
Sven Gemballa2 & Robert E. Shadwick1
Earth’s core formation. Geochim. Cosmochim. Acta 65, 1821–1832 (2001). 1
3. Righter, K., Drake, M. J. & Yaxley, G. Prediction of siderophile element/silicate partition coefficients to Marine Biology Research Division, Scripps Institution of Oceanography,
20 GPa and 2800 8C: the effects of pressure, temperature, oxygen fugacity, and silicate and metallic University of California San Diego, La Jolla, California 92093-0202, USA
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melt compositions. Phys. Earth Planet. Inter. 100, 115–134 (1997). Department of Zoology, University of Tübingen, Auf der Morgenstelle 28,
4. Righter, K., Hervig, R. L. & Kring, D. A. Accretion and core formation on Mars: molybdenum contents D-72076 Tübingen, Germany
of melt inclusion glasses in three SNC meteorites. Geochim. Cosmochim. Acta 62, 2167–2177 (1998). .............................................................................................................................................................................
5. Anderson, D. L. Theory of the Earth (Blackwell, Boston, 1989).
6. Dreibus, G. & Wanke, H. Mars, a volatile-rich planet. Meteoritics 20, 367–381 (1985).
The evolution of ‘thunniform’ body shapes in several different
7. McSween, H. Y. Jr What we have learnt about Mars from SNC meteorites. Meteoritics 29, 757–779 groups of vertebrates, including whales, ichthyosaurs1 and sev-
(1994). eral species of large pelagic fishes2 supports the view that physical
8. Kellogg, L. H., Hager, B. H. & van der Hilst, R. D. Compositional stratification in the deep mantle. and hydromechanical demands provided important selection
Science 283, 1881–1884 (1999).
9. Garnero, E. J., Revenaugh, J., Williams, Q., Lay, T. & Kellogg, L. H. in The Core-Mantle Boundary
pressures to optimize body design for locomotion during ver-
Region (eds Gurnis, M., Wysession, M. E., Knittle, E. & Buffett, B. A.) 319–334 (Geodynamics Series tebrate evolution. Recognition of morphological similarities
28, Am. Geophys. Union, Washington, 1998). between lamnid sharks (the most well known being the great
10. Poirier, J.-P. Light elements in the Earth’s outer core: A critical review. Phys. Earth Planet. Inter. 85,
white and the mako) and tunas has led to a general expectation
319–337 (1994).
11. Hillgren, V., Gessmann, C. K. & Li, J. in Origin of the Earth and Moon (eds Canup, R. & Righter, K.) that they also have converged in their functional design; however,
245–263 (Univ. Arizona Press, Tucson, 2000). no quantitative data exist on the mechanical performance of the
12. Melosh, H. J. in Origin of the Earth (eds Newsom, H. E. & Jones, J. H.) 69–83 (Oxford Univ. Press, locomotor system in lamnid sharks. Here we examine the swim-
Oxford, 1990).
ming kinematics, in vivo muscle dynamics and functional mor-
13. Stevenson, D. J. in Origin of the Earth (eds Newsom, H. E. & Jones, J. H.) 231–249 (Oxford Univ. Press,
Oxford, 1990). phology of the force-transmission system in a lamnid shark, and
14. Gessmann, C. K. & Rubie, D. C. The effect of temperature on the partitioning of Ni, Co, Mn, Cr and V show that the evolutionary convergence in body shape and
at 9 GPa and constraints on formation of the Earth’s core. Geochim. Cosmochim. Acta 62, 867–882 mechanical design between the distantly related lamnids and
(1998).
15. O’Neill, H. S. C., Canil, D. & Rubie, D. C. Metal-oxide equilibria to 2500 8C and 25 GPa: implications
tunas is much more than skin deep; it extends to the depths of the
for core formation and the light component in the Earth’s core. J. Geophys. Res. 103, 12239–12260 myotendinous architecture and the mechanical basis for propul-
(1998). sive movements. We demonstrate that not only have lamnids and
16. Kato, T. & Ringwood, A. E. Melting relationships in the system Fe-FeO at high pressures: implications tunas converged to a much greater extent than previously known,
for the composition and formation of the Earth’s core. Phys. Chem. Miner. 16, 524–538 (1989).
17. Trønnes, R. G. Melting relations and major element partitioning in an oxidized bulk Earth model
but they have also developed morphological and functional
composition at 15–26 GPa. Lithos 53, 233–245 (2000). adaptations in their locomotor systems that are unlike virtually
18. Trønnes, R. G. & Frost, D. J. Peridotite melting and mineral-melt partitioning of major and minor all other fishes.
elements at 22–24.5 GPa. Earth Planet. Sci. Lett. 197, 117–131 (2002). During their 400 million years of independent evolution, sharks
19. Li, J. & Agee, C. B. Element partitioning constraints on the light element composition of the Earth’s
core. Geophys. Res. Lett. 28, 81–84 (2001).
and bony fishes have diverged in many fundamental aspects of their
20. Rubie, D. C., Melosh, H. J., Reid, J. E., Liebske, C. & Righter, K. Mechanisms of metal-silicate anatomy and physiology. However, two groups of dominant open-
equilibration in the terrestrial magma ocean. Earth Planet. Sci. Lett. 205, 239–255 (2003). ocean predators, the lamnid sharks and the tunas, even when looked
21. Herzberg, C. & Zhang, J. Melting experiments on anhydrous peridotite KLB-1: Compositions of
at superficially, display remarkably similar morphological special-
magmas in the upper mantle and transition zone. J. Geophys. Res. 101, 8271–8295 (1996).
22. Ohtani, E. Melting temperature distribution and fractionation in the lower mantle. Phys. Earth Planet. izations related to locomotion3–12 (Fig. 1a). The shared character-
Inter. 33, 12–25 (1983). istics in these distantly related groups that distinguish them from
23. McDonough, W. F. & Sun, S.-s. The composition of the Earth. Chem. Geol. 120, 223–253 (1995). virtually all other fish have arisen independently, probably as the
24. O’Neill, H. S. C. & Palme, H. in The Earth’s Mantle (ed. Jackson, I.) 3–126 (Cambridge Univ. Press,
Cambridge, 1998).
result of selection for fast and continuous locomotion. Moreover, in
25. Chabot, N. L. & Agee, C. B. Core formation in the Earth and Moon: new experimental constraints both lamnids and tunas, the aerobic (red) musculature that powers
from V, Cr and Mn. Geochim. Cosmochim. Acta 67, 2077–2091 (2003). cruise swimming is concentrated in a more medial (closer to the
NATURE | VOL 429 | 6 MAY 2004 | www.nature.com/nature
©2004 Nature Publishing Group 61
letters to nature
backbone) and anterior position compared with the relatively all other bony fishes4,13. Similar investigations on swimming lamnid
uniform and superficial position in other fishes; the body tempera- sharks are lacking because of the difficulty in handling such large
ture is elevated above that of the surrounding water, facilitated by and dangerous predators; thus, the dynamic properties of the
counter-current heat exchangers associated with the internal red lamnid locomotor system remain unknown. This paper presents
muscle; and the muscle segments (myotomes) are highly elongated3. in vivo quantitative measurements of swimming kinematics and
Recent studies on tunas revealed a host of unique functional muscle dynamics, and analysis of the morphology of the force-
adaptations in their locomotor system that distinguish tunas from transmission system in a lamnid shark.
First, we examined the kinematics of steady swimming in the
shortfin mako shark (Isurus oxyrinchus). Lateral displacement of the
dorsal midline as a function of body position was calculated from
dorsal video images of mako sharks swimming under controlled
conditions in a swim tunnel (Fig. 1b; see also Supplementary
Video). Descriptions of undulatory swimming modes in fishes are
based on the proportion of the body that participates in the lateral
thrust-producing movements14, and can be distinguished by differ-
ences in patterns of lateral displacement along the body, as shown in
Fig. 1c. Compared with other teleosts, tunas exhibit the least
undulatory (thunniform) mode of locomotion, in which lateral
movements are largely confined to the caudal region where body
mass is reduced by tapering. The lateral displacement data pre-
sented here show that the lamnid shark kinematically resembles
tuna more than other sharks15 or subcarangiform teleosts: the
degree of lateral motion along the mako shark’s body from ,0.4L
to ,0.8L (where L is total body length) is relatively small, demon-
strating that lamnids swim using a thunniform-like mode. The
amplitude of lateral motion increases substantially beyond ,0.8L
where the body tapers to the narrow caudal peduncle. Lamnids, like
tunas, have the least lateral motion in the mid-body region where
the bulk of the muscle resides and have a reduced body mass in the
caudal region where lateral amplitudes are high, both being features
that match predictions for enhancing hydromechanical efficiency of
swimming9.
Because lamnids have both internal red muscle and a thunni-
form-like swimming mode, we tested the possibility that shortening
of the red muscle would be physically uncoupled from deformation
of the adjacent skin, backbone and white muscle, a unique func-
tional property of red muscle that has been observed so far only in
tunas. Whereas in most teleosts superficial red muscle fibres con-
tract sequentially to cause a posteriorly travelling wave of local body
bending16–18, the internal position of red muscle in tunas allows
them to abandon this pattern of undulation and adopt a novel
mechanism to project red muscle action to posterior regions of the
body4,19, thereby facilitating thunniform kinematics. In the mako
shark we used sonomicrometry to record instantaneous muscle
segment length changes during steady swimming as well as during
passive, simulated swimming movements induced under anaesthe-
sia. The temporal relationship between red and white muscle
shortening was measured to determine whether the action of
these two muscle masses is synchronized, as in most fish, or
uncoupled, as in tunas. During passive swimming movements,
Figure 1 Features of thunniform body shape and patterns of lateral undulation during peaks in red muscle strain (that is, relative length change) were in
steady swimming. a, Thunniform body shape in lamnid sharks25 (right) and tunas26 (left). phase with peaks in adjacent white muscle strain (Fig. 2a). Thus,
Note the highly streamlined fusiform body shape that minimizes pressure drag, stiff, when the body bends passively red muscle shortens synchronously
high-aspect-ratio hydrofoil caudal fin that produces thrust by a hydrodynamic-lift with the surrounding white muscle and skin, as one would expect.
mechanism, and dorsoventrally flattened and enlarged caudal keel that decreases drag In contrast, during active swimming the peaks in red muscle strain
produced by lateral movement of the peduncle6–8. b, Dorsal image of steady swimming were delayed relative to peaks in white muscle strain (Fig. 2b). By
I. oxyrinchus. Scale bar: 10 cm. c, Lateral displacement, relative to the amplitude of lateral cross-correlation analysis we determined that the mean phase shift
motion at the tail tip, versus axial position in the mako shark (n ¼ 5; red symbols), tuna between simultaneous recordings of red and white muscle strain was
(red dashed line27), leopard shark (black solid line15) and subcarangiform teleosts 90 ms (or ,10% of the tail-beat cycle), with one individual as high
(black dashed line; modified from ref. 13). This graph emphasizes differences in as 174 ms (,17% of tail-beat cycle). The observed phase shift
displacement in the mid-body where most of the variation among swimming modes indicates that during steady swimming the red muscle is indeed
occurs. Comparison of the mako shark and tuna illustrates the similarity in their swimming physically uncoupled from the surrounding tissues and contracts in
mode, where lateral undulations are largely confined to the caudal region, indicated by phase with body bending at a more posterior location.
shading in dorsal outlines. The reduction in lateral motion in the mid-body region afforded On the basis of a wave velocity of about 1 l s21 in sharks
by their internal red muscle and modified force-transmission system is evident when swimming with a tail-beat frequency of about 1 Hz, the red muscle
comparing the mako shark and tuna to sharks and bony fishes with less-specialized in the mid-body region will be shortening in phase with bending of
swimming modes such as the subcarangiforms shown here. the backbone 10–17% closer to the tail. A consequence is that
62 ©2004 Nature Publishing Group NATURE | VOL 429 | 6 MAY 2004 | www.nature.com/nature
 letters to nature
during short portions of each contraction cycle the red muscle will deep red muscle shortens and transmits force and displacement to
be lengthening while the adjacent white fibres are shortening, and more posterior regions of the body rather than effecting local
vice versa. The loose sheath of connective tissue that surrounds the bending4,19. Thus, the same mechanism enables tunas and lamnid
red muscle mass (see Fig. 3d) may facilitate this shearing. These sharks to swim with the relatively stiff-bodied thunniform mode of
results are remarkably similar to those described in tunas, where the propulsion; even though the bulk of aerobic muscle is located more

Figure 2 Simultaneous recordings of muscle strain (segment length change/mean length) During active swimming, as verified by red muscle activity (EMG trace), shortening in the
of red (red trace) and adjacent white (grey trace) muscle during passive simulated red muscle is delayed relative to the white muscle and is therefore in phase with lateral
swimming movements (a) and active steady swimming (0.5 l s21) (b) in the mako shark. motion in more posterior positions.

Figure 3 Collagenous architecture of myosepta of I. oxyrinchus. a, Oblique view focusing from skin; dotted line, excision line from remaining dorsal part of the myosepta, equivalent
on the hypaxial part between 0.54L and 0.74L (coloured inset). The elongated anterior to the dotted line in a; white arrowheads, intersection line of myosepta and loose
pointing cone (AC) of one myoseptum is shown. It intersects with the red musculature connective tissue surrounding red muscle. c, d, Transverse sections of left side.
(pale red area) and contains the hypaxial lateral tendon (dark red). The hypaxial lateral Concentric rings of myosepta indicate nesting anterior pointing cones. c, Fresh section,
tendon extends between the tip of the anterior pointing cone and the ventral posterior 0.6L, showing red muscle with sections of hypaxial lateral tendons (white) within the red
cone (VPC). The hypaxial lateral tendon of a more anterior myoseptum is also shown muscle. d, Histological section at 0.54L. Red muscle is separated from surrounding white
without its myoseptal sheet. The anterior part of this tendon is cut at its intersection with muscle by a sheath of loose connective tissue. Numbers 1–12 indicate anterior portions of
the transverse plane (blue). b, Excised area of myosepta between the anterior pointing 12 hypaxial lateral tendons present in red muscle, whereas numbers 13–24 indicate
cone and ventral posterior cone flattened out under polarized light. Pathways of posterior portions of 12 additional hypaxial lateral tendons present in white muscle,
collagenous structures are shown in white. The hypaxial lateral tendon extends between meaning that a single tendon covers 24 segments. The inset shows a detailed view of red
the red arrows. Dashed line, excision line from vertebral axis; thick white line, excision line muscle and hypaxial lateral tendons (stained orange).
NATURE | VOL 429 | 6 MAY 2004 | www.nature.com/nature
©2004 Nature Publishing Group 63
letters to nature
anteriorly than in less derived species, the lateral motion it produces transport chamber equipped with circulating aerated sea water. Once at SIO, the sharks
were placed into a large 3,000-l swim tunnel for an acclimation period of several hours
is primarily focused to the caudal region. before experimentation. All procedures in capture, maintenance and experimentation
Our morphological investigations demonstrate that the anatomi- followed the guidelines of the University of California, San Diego Institutional Animal
cal specializations associated with the force-transmission system are Care and Use Committee.
also convergent. We used a new combination of techniques to
explore the three-dimensional morphology of the tendinous con- In vivo muscle dynamics
nective tissue linkages (myosepta) that transmit muscular forces to To examine the dynamics of red and white muscle contractions during swimming, we used
electromyography (EMG) and sonomicrometry, a technique for measuring distances in
the skin and backbone, and their relationship to the internal red which piezoelectric crystals transmit and receive ultrasonic pulses. Pairs of
muscle in the mako shark. sonomicrometric crystals were implanted into the deep red and adjacent white muscle to
In principle, the three-dimensional shape of myotomes and their record instantaneous changes in muscle segment length (strain) during active periods of
associated myosepta in mako sharks resembles the regular pattern in steady swimming as well as during passive, simulated swimming movements induced
under anaesthesia. Surgery was performed on anaesthetized individuals partially
gnathostome fishes20, which includes a main anterior cone and a submerged in a seawater bath according to procedures described previously15. Crystal
dorsal and ventral posterior cone (see Supplementary Fig. 1 for pairs were implanted approximately 15 mm apart along the longitudinal axis of the body
myoseptal parts of gnathostomes and mako sharks). Additionally, in and the leads were loosely anchored to the skin with surgical sutures. To verify the passive
mako sharks two secondary anterior cones are present at the dorsal- and active states of the red muscle, electrical activity was recorded using pairs of electrodes
implanted approximately 2 mm apart directly bisecting the crystal pairs. After surgery, the
and ventral-most part of the myoseptum. The red muscle is situated sharks were placed into the swim tunnel and allowed to recover before data collection. In
in the lower part of the main anterior cone (Fig. 3a; see also the recovery period we recorded red and white muscle strain during passive, simulated
Supplementary Fig. 1d, e) where its fibres insert into the collagenous swimming movements induced by gentle side-to-side motions of the centre of mass that
myoseptum. In particular, red muscle fibres insert into the anterior generated body undulation. Additionally, we recorded and analysed 30–50
consecutive tail-beat cycles for each individual while the shark swam steadily at
half of a myoseptal tendon (Fig. 3a). This tendon runs from the tip
approximately 0.5 l s21. To measure the relative timing of red and white muscle
of the main anterior cone through the red muscle towards its end strain (phase shift), a cross-correlation analysis was performed using waveforms
within the white muscle at the ventral posterior cone (Fig. 3a, b). It containing approximately ten consecutive tail-beat cycles. Mean phase shift presented
clearly represents the homologue of the hypaxial lateral tendon in in the text represents a mean of five individuals. Sonomicrometric and EMG signals
gnathostome fishes (Supplementary Fig. 1). In mako sharks, this were recorded at 500 Hz.
To correlate measurements of local muscle activation and strain with patterns of body
tendon is extremely prominent and elongated when compared bending, five mako sharks were videotaped while swimming against a current of known
with other fishes. In fact, myoseptal tendons as long and as velocity in the swim tunnel. To synchronize the collection of sonomicrometric, EMG and
distinct as those associated with the red muscle in the mako shark video recordings, a flashing red diode was recorded in the video sequences and its
have never been reported in any shark species. We measured excitation voltage was recorded with the sonomicrometric and EMG data. Kinematic
analysis follows procedures described previously15,24.
tendon lengths as long as 0.19L in the posterior region of the
body (Supplementary Fig. 1e). The sonomicrometric results Morphology
suggest that the action of the red muscle is directed posteriorly We used a combination of clearing and staining, microdissection, polarized light
along the body by 10–17%. The measured tendon lengths accord microscopy, standard histology and computer-based three-dimensional reconstruction to
well with the values predicted from sonomicrometry, suggesting explore the three-dimensional morphology of the tendinous connective tissue linkages
(myosepta). A small body segment (0.54–0.55L) of a formalin-fixed mako specimen
that the hypaxial lateral tendon is responsible for transmitting red (65 cm total length) was prepared for standard histology (paraffin embedding; Azan–
muscle forces posteriorly. The prominent tendons of the posterior Domagk staining, slice thickness of 15 mm). The two remaining parts (0–0.54L and
body are gradually developed along a rostrocaudal gradient from 0.55–1.00L) were carefully skinned, stained for cartilage with Alcian blue 8GX (Merck)
shorter (,0.06L; Supplementary Fig. 1d) and less distinct hypax- and then cleared according to a recently described procedure20. Microdissections on the
myoseptal system were carried out using fine microsurgery tools. Myosepta or parts of
ial lateral tendons of anterior myosepta to longer tendons in the
myosepta from all body regions were removed subsequently. Three-dimensional shape of
posterior. the myosepta was documented by a camera lucida, and tendon lengths and rostrocaudal
In tunas, distinct and elongated tendons have also been discov- extensions of complete myosepta were measured in situ. Removed myosepta were
ered and have been hypothesized to transfer forces from the red photographed under polarized light to visualize the collagen fibre pathways and tendons
muscle to the axial skeleton, and thus provide the anatomical basis (Zeiss Stemi 2000C with Fuji X digital camera HC300Z; 1,000 £ 1,450 pixels).
Additionally, the distribution of red muscle and its relation to myoseptal cones along the
for force transmission from the anterior to the caudal region21. As body was examined. A three-dimensional reconstruction was obtained from histological
in mako sharks, the available length measurements and sonomicro- sections. Major landmarks (vertebrae, neural arches, vertical septum, abdominal cavity,
metric data are in good accordance (0.18L experimentally and 0.16L tip of main anterior, secondary anterior and ventral posterior cone, sections of tendons,
morphologically)22. Although in tunas the primary force-transmit- position of red muscle) were digitized and aligned using SurfDriver 3.5.3. Maxon Cinema
4D (Release 6) was used for choosing an adequate perspective and rendering. The obtained
ting tendons are in the horizontal septum, in the mako shark, as in three-dimensional view was edited by Adobe Photoshop (final shading, adding of
other sharks23, we found the horizontal septum to be reduced in the myoseptal shape).
posterior half of the body. Instead, the primary linkage to the tail Received 23 January; accepted 25 February 2004; doi:10.1038/nature02435.
appears to be the hypaxial lateral tendons. Interestingly, although
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tuna Katsuwonus pelamus: timing of red muscle shortening and body curvature during steady realization of fitness optima6. Unfortunately, evidence for this type
swimming. J. Exp. Biol. 202, 2139–2150 (1999). of conflict is rare. However, recent empirical work in Drosophila
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Lond. B 270, 1229–1235 (2003).
melanogaster showed that adult relative fitness was negatively
21. Westneat, M. W., Hoese, W., Pell, C. A. & Wainwright, S. A. The horizontal septum: mechanisms of correlated between the sexes, even though there was a positive
force transfer in locomotion of scombrid fishes (Scombridae, Perciformes). J. Morphol. 217, 183–204 genetic correlation for fitness earlier in development4. The authors4
(1993).
further predicted that if these results were applicable outside
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23. Gemballa, S., Hagen, K., Röder, K., Rolf, M. & Treiber, K. Structure and evolution of the horizontal Drosophila, a female mating bias for high-quality mates would
septum in vertebrates. J. Evol. Biol. 16, 966–975 (2003). produce at best only average-quality daughters.
24. Jayne, B. C. & Lauder, G. V. Speed effects on midline kinematics during steady undulatory swimming We addressed this prediction in A. socius by examining the genetic
in largemouth bass, Micropterus salmoides. J. Exp. Biol. 198, 585–602 (1995).
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correlation between a sire’s field-determined mating success and his
Western Central Pacific (eds Carpenter, K. E. & Niem, V. H.) 1274–1278 (FAO, Rome, 1998). son’s mating success and daughter’s reproductive success. We chose
26. Joseph, J., Klawe, W. & Murphey, P. Tuna and Billfish—Fish Without A Country 1–69 (Inter-American these offspring variables on the assumption that they are accurate
Tropical Tuna Commission, La Jolla, California, 1988).
predictors of next-generation fitness. Previous work suggests that
27. Knower, T. Biomechanics of Thunniform Swimming Thesis, Univ. California, San Diego (1998).
A. socius females mate with larger males to gain a larger haemo-
Supplementary Information accompanies the paper on www.nature.com/nature. lymph-based nuptial gift. This gift is obtained by chewing a
specialized spur on the male hind tibia during copulation7,8. There-
Acknowledgements We thank A. Biewener, J. Gosline, J. B. Graham, S. Vogel and N. Holland for fore, the condition of the spur (chewed or unchewed) indicates a
discussion and reviews. Funding was provided by NSF and UC Regents. male’s mating history (successful or unsuccessful): chewing beha-
viour is rarely uncoupled from sperm transfer. Spur condition also
Competing interests statement The authors declare that they have no competing financial
interests.
seems to be age-independent because spur categories persist
throughout a breeding season that is characterized by little new
Correspondence and requests for materials should be addressed to J.D. ([email protected]). male recruitment once a cohort emerges8. Use of an ‘aggregate’
indicator, such as mating success, is important because it represents
the sum of interacting male traits9, overcoming the implicit weak-
ness of the traditional ‘simple’ indicator approach1–3.
To estimate the sire–offspring correlations, we mated 47 wild-
.............................................................. caught sires (25 successful and 22 unsuccessful) to 98 wild-caught
females and reared their offspring. Sires were caught mid-breeding
Female mating bias results season and females were collected as late instar nymphs earlier in the
season to ensure their virginity; on average there were two females
in conflicting sex-specific per sire. Males that had mated in the field were larger than unmated
offspring fitness males (F 1,45 ¼ 7.25, P ¼ 0.0099) and there was no female size
difference between sire groups (F 1,96 ¼ 0.01, P ¼ 0.9294). From
each female family, two or three sons (n ¼ 220 total males) were
Kenneth M. Fedorka* & Timothy A. Mousseau
separately placed into a mating arena with a randomly chosen,
Department of Biological Sciences, University of South Carolina, Columbia, unrelated male and female taken from other sire families (see
South Carolina 29208, USA
* Present address: Department of Genetics, University of Georgia, Athens, Georgia 30602, USA
.............................................................................................................................................................................
Indirect-benefit models of sexual selection assert that females Table 1 Genetic correlation between a sire’s phenotype and offspring variables
gain heritable offspring advantages through a mating bias for Trait Sire mating success Sire size
males of superior genetic quality. This has generally been tested
n rG P rG P
by associating a simple morphological quality indicator (for .............................................................................................................................................................................
example, bird tail length) with offspring viability1. However, Son mating success 4.7 0.38 0.0076 0.06 0.7679
selection acts simultaneously on many characters, limiting the Daughter reproductive 6.9 2 0.36 0.0164 20.02 0.9280
Hatching* 545.9 0.01 0.9813 0.07 0.7549
ability to detect significant associations, especially if the simple Survivorship* 133.8 0.08 0.5708 0.03 0.8971
indicator is weakly correlated to male fitness2,3. Furthermore, Son development* 21.2 20.02 0.9134 0.01 0.9785
Daughter development* 23.8 0.03 0.8218 0.01 0.5381
recent conceptual developments suggest that the benefits gained Son size* 13.8 0.08 0.5924 0.17 0. 9670
from such mating biases may be sex-specific because of sexually Daughter size* 15.0 20.16 0.2737 0.00 0.9990
.............................................................................................................................................................................
antagonistic genes that differentially influence male and female * Juvenile viability variable.
reproductive ability4. A more suitable test of the indirect-benefit Two sire phenotypes were examined, including sire mating success and sire size. n represents the
average number of individuals per sire family. Bold values remain significant after a sequential
model would examine associations between an aggregate quality Bonferroni. P-values corrected within each sire phenotype (mating success and size) and within
indicator1,3 (such as male mating success) and gender-specific each fitness stage (that is, adult fitness and juvenile viability).

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