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Am. Midl. Nat. 143:212–225
Selection on a Sexually Dimorphic Trait in Ecotypes within
the Hyalella azteca Species Complex
(Amphipoda: Hyalellidae)
GARY A. WELLBORN1
Department of Zoology and Biological Station, University of Oklahoma, Norman 73019
ABSTRACT.—Many amphipods (Crustacea: Amphipoda) exhibit sexual dimorphism in the
size of a paired chelate appendage, the gnathopods. As with sexually dimorphic weapons
and ornaments in other taxa, little is known of the evolutionary processes underlying species
variation in the dimorphism. In this study I examined males of two ecotypes of freshwater
amphipods in the genus Hyalella to determine (1) the degree and form of reproductionmediated selection acting on gnathopod size, (2) the importance of fluctuating asymmetry
in gnathopods for mating success and (3) differences between ecotypes in gnathopod size.
I examined sexual selection arising from differential success in forming mating pairs and
natural selection due to success in mating with larger, more fecund females. The two ecotypes
differed in the pattern of selection acting on gnathopod size. The small-bodied ecotype did
not experience significant selection on gnathopod size in either selection episode. In contrast, the large-bodied ecotype experienced significant sexual selection for increased gnathopod size (relative to overall body size) and experienced selection for smaller gnathopod
size during the natural selection episode. Fluctuating asymmetry in gnathopods occurred at
relatively low levels and was not related to pairing success in either ecotype. The two ecotypes
differed significantly in gnathopod size relative to body size, with the small-bodied ecotype
having gnathopods approximately 18% larger than those of the large-bodied ecotype. These
results, together with previous results, suggest that gnathopod size is important in the mating
success of males of the large-bodied ecotype, but not the small-bodied ecotype, and that
ecotype differences in the level of the sexual dimorphism may have evolved for reasons
unrelated to mating success.
INTRODUCTION
Across an extensive diversity of animal taxa males often have elaborated sexually-dimorphic traits such as ornaments and weapons (e.g., Darwin, 1871). Despite the prevalence of
these traits, we are only beginning to understand the full scope of functional and evolutionary mechanisms underlying their evolution (Andersson, 1994). One approach for evaluating the function and evolution of these traits is to examine how the traits influence
reproductive success of males in different populations or in closely related species (Endler,
1983, 1987; Zeh, 1987; Wellborn, 1995b; Fairbairn and Preziosi, 1996). Such comparative
studies can help to identify ways that evolution of dimorphic traits differ under different
environmental or selection regimes, providing clues to the mechanisms that may generate
population and species variation in the traits.
In many amphipod crustaceans one or both of the first two thoracic appendages, called
gnathopods, are larger in males than in females (Bousfield, 1973; Conlan, 1991). The presence of sexually dimorphic gnathopods is associated with taxonomic affiliation at the level
of superfamilies (Conlan, 1991), indicating an important phylogenetic component for the
dimorphism. In addition to phylogeny, natural selection based on functional significance
of gnathopods is also likely to shape patterns of gnathopod dimorphism within taxonomic
1
e-mail: [email protected]; Telephone: (405) 325-1421; FAX: (405) 325-6202
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lineages. Support for this assertion is twofold. First, amphipods exhibit substantial variation
in the degree of dimorphism among species within amphipod superfamilies (Conlan, 1991).
For species within the Talitroidea, the group that includes the subjects of this study, the
coefficient of variation in the mean dimorphism in gnathopod perimeter is 62% (calculated
from Figure 5 in Conlan, 1991). Second, gnathopods are often substantially enlarged in
males, and thus are likely to be costly to produce and maintain. Because costly traits are
unlikely to be selectively neutral, they are presumably maintained by selection.
Although a functional role for enlarged gnathopods has been described or suggested for
a few amphipod species (e.g., Hartnoll and Smith, 1978; Mattson and Cedhagen, 1989;
Conlan, 1991), a general understanding of their function in male amphipods is lacking.
Proposed or demonstrated functions of enlarged gnathopods include use in intrasexual
contests during precopulatory mate guarding (Strong, 1973), intraspecific territorial interactions (Mattson and Cedhagen, 1989), intersexual courtship displays (Mattson and Cedhagen, 1989) and assessment of female quality (Hartnoll and Smith, 1978; Borowsky and
Borowsky, 1987; Dick and Elwood, 1989).
The Hyalella azteca species complex.—Hyalella (Amphipoda: Talitroidea: Hyalellidae) are
distributed across many lacustrine habitats throughout North America and exhibit substantial genetically based differentiation among populations in body size (Strong, 1972; Wellborn, 1994a), behavior (Strong, 1973; Wellborn, 1995b; Thomas et al., 1997), life history
(Strong, 1972; France, 1992; Wellborn, 1994b) and morphology (Stevenson and Peden,
1973; Cole and Watkins, 1977). Although divergent morphotypes are often grouped within
the taxon H. azteca (but see descriptions of two North American endemic species derived
from H. azteca [Stevenson and Peden, 1973; Cole and Watkins, 1977]), the level of phenotypic and genetic divergence observed among populations and apparent lack of interfertility between some ecotypes suggests H. azteca is a species complex (Wellborn, 1995a;
McPeek and Wellborn, 1998). The general lack of qualitative morphological differentiation
(Strong, 1972; Wellborn, 1995a), however, suggests recent diversification within the taxon.
In Michigan there is a striking pattern of habitat-specific morphological and life history
variation between two species in the Hyalella azteca species complex (Wellborn, 1994a,
1995b; McPeek and Wellborn, 1998). For convenience I refer to these probable species as
ecotypes. This evolutionary diversification is driven by heterogeneity among habitats in the
form of size-biased predation mortality experienced by the amphipods (Wellborn, 1994a,
1995a). Fishless habitats contain a large-bodied ecotype and habitats with centrarchid fish
contain a small-bodied ecotype (Wellborn, 1995a). The body size difference between the
ecotypes is appreciable, with adults differing by approximately 35% in head length (Wellborn, 1995a), or a difference of approximately 75% in dry mass (based on length-mass
regression in Edwards and Cowell, 1992). The ecotypes also differ in life history. Compared
to the small-bodied ecotype, individuals of the large-bodied ecotype mature at a larger size
and exhibit a lower reproductive effort (Wellborn, 1994a). Hyalella in the two habitat types
experience qualitatively different regimes of size-biased predation (Wellborn, 1994a), and
the observed body size and life history differences are consistent with those expected under
these disparate mortality schedules (Roff, 1992; Stearns, 1992; Taylor and Gabriel, 1992).
The difference in direction of size-biased predation mortality observed for Hyalella in
fish-containing and fishless habitats may have important consequences for the evolution of
mating behavior. Selection for mortality from predation may interact with mating systems
to influence patterns of reproductive success and sexual selection (Endler, 1983; Houde
and Endler, 1990; Wellborn, 1995b). In a previous study of two Hyalella ecotypes in southeast Michigan I found that the influence of gnathopod size on male reproductive success
differed between ecotypes (Wellborn, 1995b). In the large-bodied ecotype male reproduc-
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tive success increased monotonically with gnathopod size, but in the small-bodied ecotype
population mating success did not depend on gnathopod size (Wellborn, 1995b). Thus
sexual selection for conspicuous traits could be constrained by mortality selection from
predatory fish that rely on visual cues for prey detection.
Hyalella life cycle and mating biology.—Hyalella amphipods are widely distributed in permanent freshwater habitats across North America and often occur at high densities in aquatic vegetation (Bousfield, 1973; De March, 1981; Wellborn, 1994a). Juveniles pass through
approximately seven instars before reaching maturity. Adults continue to molt and grow
throughout their lives, though growth rates decline at larger adult body sizes (Wellborn,
1994b). Females produce a clutch of eggs at each molt (Cooper, 1965; Strong, 1973). Reproduction is sexual and females have no mechanism for sperm storage. Fertilized eggs are
carried in a ventral brood chamber, the marsupium, and hatch just before the female’s
molt. Before the female’s molt males use their anterior gnathopods (not enlarged) to grasp
the female’s second coxal segment in a precopulatory mate-guarding behavior (Borowsky,
1984). Pairs remain attached with the male dorsal to the female until the female’s molt, at
which time first-instar offspring are released and the new clutch of eggs is fertilized by
guarding males as eggs pass into the marsupium. Pairs separate after fertilization.
In Hyalella only the posterior gnathopods are enlarged, and these are approximately 15
times larger in males than females. Males do not use posterior gnathopods to grasp females
during precopulatory mate guarding (Borowsky, 1984). Although enlarged gnathopods may
be important in male-male conflicts in Hyalella, their use in displacing a paired male appears to be rare since two studies examining interactions between paired and unpaired
males reported that no takeovers occurred (Strong, 1973; Wen, 1993).
Observations of pairing behavior in Hyalella suggest that females have substantial control
in pair formation. Male Hyalella generally attempt to pair with any individual encountered,
regardless of sex or reproductive condition (Strong, 1973; pers. obs.). Females, however,
appear selective and only accept males during the later stages of their molt cycle (Strong,
1973). When males encounter and attempt to pair with a nonreceptive female, the female
alternately curls and extends her body vigorously, apparently dissuading the male (Strong,
1973; pers. obs.). Receptive females do not exhibit this thrashing behavior.
Here I explore the role of gnathopod characteristics in male reproductive success by
measuring aspects of sexual selection (pairing success) and natural selection (success in
mating with larger, more fecund females) on gnathopod size in the two amphipod ecotypes.
Gnathopod size is examined because such sexually dimorphic traits may often be maintained by sexual or reproduction-based natural selection (Andersson, 1994), and dimorphic
traits may respond to population or species differences in countervailing selection pressures
(Endler, 1983; Houde and Endler, 1990; Wellborn, 1995b). Also, I explore patterns of fluctuating asymmetry of gnathopods and ask whether fluctuating asymmetry is related to male
mating success. Fluctuating asymmetry refers to small random deviations from perfect symmetry in bilateral traits and reflects the degree of developmental instability of the trait
(Watson and Thornhill, 1994). Fluctuating asymmetry may be important in studies of sexual
selection in at least two ways. First, the degree of a male’s deviation from bilateral symmetry
may serve as an epigenetic indicator of male quality and thus influence his success in
intersexual or intrasexual interactions (Møller, 1992; Møller and Pomiankowski, 1993; Watson and Thornhill, 1994). Second, if there is strong selection for larger trait size fluctuating
asymmetry may incidentally increase because selection should reduce the influence of modifier genes that may constrain increases in trait size (Møller, 1993).
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METHODS
Study habitats and collection procedure.—George Pond (428289N, 848019W) contains a population of the large-bodied Hyalella ecotype (Wellborn, 1995a). It is a small, isolated, permanent pond dominated by the aquatic plant Myriophyllum and is often covered extensively
with duckweed (Lemna). George Pond does not have predatory fish, but does contain
predatory salamanders and invertebrates (principally larval odonates). South Lake
(428249N, 848049W) contains a population of the small-bodied Hyalella ecotype and is a
moderate-sized lake with much littoral emergent (Typha) and submerged (Myriophyllum,
Potomogeton) vegetation. South Lake contains predatory fish, including bluegill (Lepomis
macrochirus), an important consumer of Hyalella (Wellborn, 1994a).
I collected paired and unpaired Hyalella in littoral vegetation in George Pond on 9
August and South Lake on 28 July 1995, a time when Hyalella populations in this region
have large populations, overlapping generations and substantial size variation. To collect
both mating pairs and unpaired individuals, I swept a small, fine-mesh, dip net through the
vegetation, lifted it from the water and, before water had completely drained from the net,
emptied the sample into a white tray filled with pond or lake water. I collected and individually preserved all precopulatory pairs, which were easily visible in the tray. All remaining
amphipods in the tray (i.e., unpaired individuals) were preserved collectively. Approximately 30 such samples were collected per habitat. It is unlikely that the disturbance created
by this sampling process lead to separation of some pairs before collection. I have commonly
observed that substantially more disturbance, such as prodding or placing the pair on a dry
surface, is required to cause separation (see also Ward, 1988).
Analysis of selection on gnathopod characteristics.—Gnathopod characteristics may affect
the reproductive success of males by influencing (1) the success of males in forming precopulatory pairs with females and (2) the success of males in mating with larger, more
fecund females. Female size is correlated with fecundity (described below, and see Strong,
1972; Wellborn, 1994a), and thus the expected number of eggs a male will fertilize. Relative
success in forming precopulatory pairs and pairing with larger females represent episodes
of sexual and natural selection, respectively (Arnold and Wade, 1984a, b; Ward, 1988).
I examined selection on gnathopod size. Absolute gnathopod size is not an appropriate
metric for use in selection analyses in Hyalella because body growth, including gnathopod
growth, continues after maturation (Conlan, 1991; Wellborn, 1994b). Thus, age variation
(and its correlate, gnathopod size) may contribute to variance in male mating success in a
cross sectional study, but this variation will not necessarily denote any contribution to variation in lifetime mating success (Arnold and Wade, 1984b). I attempted to circumvent this
difficulty by using residual deviations in gnathopod size (calculated from linear regression
of gnathopod size on body size) as data in my analyses (Wellborn, 1995b; see also Jones et
al., 1992). Therefore, strictly I examine patterns of selection on this residual deviation in
gnathopod size. That is, I ask whether fitness variation in males is associated with possession
of larger or smaller gnathopods relative to body size. Size of posterior gnathopods in males
was measured as the maximum width of the propodus (it is the propodus, or distal segment,
that is enlarged in males), and the larger of the left and right gnathopods was used as an
individual’s size in the calculation of residuals. As an index of body size in regressions, I
used the length of the head capsule, a metric highly correlated with total length in Hyalella
(Edwards and Cowell, 1992). Using a stereomicroscope fitted with an ocular micrometer, I
measured characters to the nearest 0.022 mm, a resolution of approximately 3–4% of gnathopod width and head length. The minimum body size of males included in analyses was
the size of the smallest paired individual in each habitat. I measured characters on all paired
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males. For unpaired males I counted all adult males, measured characters on a random
sample of these males, then used proportional occurrence of paired and unpaired males
to weight the regression parameters in calculation of residual gnathopod size for the population as a whole.
I calculated linear selection gradients as regression coefficients from regression of relative
fitness on standardized character values (Lande and Arnold, 1983). Relative fitness for each
individual was calculated as w9 5 w/w̄, where w is absolute fitness and w̄ is the average
absolute fitness across the population. For pairing success, absolute fitness of individuals
was 1 for paired males and 0 for unpaired males (Ward, 1988; Fairbairn and Preziosi, 1996),
and average absolute fitness across the population was thus the proportion of males in
precopulatory pairs. For success in mating with larger females, absolute fitness of an individual was the expected number of eggs to be fertilized by a paired male and mean fitness
was the average expected fertilization success for all paired males. The expected number
of eggs to be fertilized by each male was based on the head length of his mate. I calculated
the expected fecundity for females of a given head length by regression of egg number on
female head length for a random sample of unpaired females in the collections. Fecundity
was not measured directly in mated females because paired females, which are nearing a
molt, often release hatched offspring before pairing and thus provide an unreliable estimate
of fecundity. Statistical significance of selection gradients was determined as their significance in the linear regressions.
Fluctuating asymmetry was calculated as the size difference between an individual’s larger
and smaller gnathopod divided by the size of the larger gnathopod (i.e., the proportional
difference in size between the two gnathopods). I used protocols suggested by Pomeroy
(1997) to test for the presence of asymmetry and to determine the form of asymmetry
exhibited by the amphipods. This analysis indicated that both ecotypes had significant asymmetry in gnathopod size (P , 0.001 in both ecotypes) and that asymmetry was not significantly directional (P . 0.39 in both ecotypes), indicating true fluctuating asymmetry. To
determine whether fluctuating asymmetry influenced male mating success, I compared
mean fluctuating asymmetry of paired and unpaired males using analysis of variance.
I used analysis of covariance (head length as covariate) to determine whether the two
ecotypes differ in gnathopod size when adjusted for overall differences in body size. I also
evaluated broader patterns of ecotype-related differences in gnathopod size by combining
data from the current study with information from four additional small-bodied and three
additional large-bodied populations (based on reanalysis of data reported in another form
in Wellborn, 1995a). The populations used in the broader analysis are all within 20 km of
each other and are described in Wellborn (1993, 1995a). To adjust for general body size
differences among populations and ecotypes, I first used analysis of covariance (head length
as covariate) to derive for each individual the sum of its population’s adjusted mean gnathopod size and that individual’s residual deviation from the adjusted mean. These values
were used as variates to test for differences between ecotypes and among populations within
ecotypes in a nested analysis of variance.
RESULTS
The proportion of males in precopulatory pairs differed significantly between ecotypes
(Fisher’s exact test, P , 0.001), with 36.6% (56 of 153) of George Pond males paired,
compared with 14.5% (55 of 379) of South Lake males. This difference reflects a difference
in duration of precopulatory mate guarding (Strong, 1973; Wellborn, 1995b). The difference in precopulatory duration gives rise to a substantial disparity in the opportunity for
selection (Table 1). Opportunity for selection is quantified as the variance in relative fitness
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TABLE 1.—Opportunity for selection for the small-bodied ecotype in South Lake and the large-bodied
ecotype in George Pond for success in forming precopulatory pairs (sexual selection) and success in
mating with larger, more fecund females (natural selection). See text for explanation of opportunity
for selection. Sample sizes are given in parentheses
South Lake
George Pond
Sexual selection episode
Natural selection episode
8.595 (379)
1.542 (153)
0.118 (55)
0.145 (56)
(Arnold and Wade, 1984a), and is a measure of the upper limit that selection may obtain.
Intuitively, the shorter duration of precopulatory guarding for South Lake males affords
individual males the potential to mate more frequently, giving rise to higher variance in
relative fitness and a higher possible magnitude of sexual selection. The opportunity for
selection in the egg fertilization episode was much smaller and was similar for both ecotypes.
The expected fecundity of females used in calculations of selection gradients was determined for a random sample of females collected in the study. These regressions were, for
George Pond expected eggs 5 female head length 3 86.4 2 48.7 (n 5 125; r2 5 0.61, P ,
0.001) and for South Lake expected eggs 5 female head length 3 35.5 2 11.7 (n 5 71; r2 5
0.61, P , 0.001).
The pattern of selection on gnathopod characters differed between ecotypes (Table 2).
Males in George Pond experienced significant sexual selection for increased gnathopod
size (Fig. 1). Gradients for natural selection due to success in pairing with larger females
were negative and significant for residual size, indicating selection for smaller gnathopod
size during this episode (Fig. 2). Total directional selection was not significant.
The sexual selection gradient for gnathopod size of males in South Lake was not significant and had large standard errors (Table 2). The broad variation in these estimates arises
from the combination of the large variation in fitness (i.e., large opportunity for selection)
and absence of a discernable relationship between gnathopod characters and fitness. Natural selection gradients due to success in pairing with larger females were not significant
and had small standard errors, indicating that selection is not operating in this episode.
Similarly, total selection was not significant.
TABLE 2.—Selection gradients (b 6 SE) for residual gnathopod size calculated for the small-bodied
ecotype in South Lake and the large-bodied ecotype in George Pond. Results are given for success in
forming precopulatory pairs (sexual selection) and success in mating with larger, more fecund females
(natural selection)
N
b6
SE
South Lake
Sexual selection
Natural selection
Total selection
122
55
122
0.26 6 0.314
0.04 6 0.056
0.34 6 0.345
George Pond
Sexual selection
Natural selection
Total selection
134
56
134
0.24* 6 0.110
0.13* 6 0.050
0.11 6 0.124
* P , 0.05
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FIG. 1.—The form of sexual selection on residual gnathopod size in George Pond males. Pairing
success is expressed as absolute fitness (paired 5 1, unpaired 5 0) and residual gnathopod size is
standardized. The solid line indicates the form of selection as estimated with the cubic spline and
dotted lines indicate bootstrapped standard errors of the estimate (Schluter, 1988). Data points are
indicated by short vertical lines (many points overlap)
Levels of fluctuating asymmetry in gnathopods were similar for South Lake (mean 6 SE
5 0.013 6 0.002) and George Pond (0.011 6 0.002) ecotypes and did not differ significantly
(Kolmogorov-Smirnov test, P 5 0.13). Overall, left and right gnathopods did not exhibit
much asymmetry within the detection limits of this study. In George Pond 72% of males
had identically-sized gnathopods and 96% had gnathopods that differed by 5% or less. In
South Lake 71% of males had identically-sized gnathopods and 89% had gnathopods that
differed by 5% or less. Fluctuating asymmetry was not related to mating success in either
George Pond (mean 6 SD for mated 5 0.014 6 0.018, unmated 5 0.008 6 0.017; P 5
0.052) or South Lake (mated 5 0.013 6 0.020, unmated 5 0.014 6 0.025; P 5 0.74).
Finally, fluctuating asymmetry was independent of body size in both South Lake (r 5 0.032,
P 5 0.729) and George Pond (r 5 0.023, P 5 0.789).
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FIG. 2.—The form of natural selection due to success in pairing with larger, more fecund females
on residual gnathopod size in George Pond males. The abscissa is the expected number of eggs fertilized by a male as determined by the size of his mate (see explanation in text) and is expressed units
of relative fitness. Residual gnathopod size is standardized. The solid line indicates the form of selection
as estimated with the cubic spline and dotted lines indicate bootstrapped standard errors of the estimate
(Schluter, 1988). Data points are indicated by a ‘1’
South Lake Hyalella have larger gnathopods, relative to body size, than do George Pond
Hyalella (Fig. 3; ANCOVA, P , 0.001). The difference between ecotypes in these two populations reflects a general difference between the ecotypes in gnathopod size (when adjusted for differences in body size). Nested analysis of variance of gnathopod size (adjusted
for population differences in overall body size) indicated that the small-bodied ecotype has
larger gnathopods than the large-bodied ecotype (P , 0.001), and that there was significant
heterogeneity in gnathopod size among populations within ecotypes (P , 0.001).
DISCUSSION
Males of the large-bodied ecotype in George Pond and the small-bodied ecotype in South
Lake differed in the pattern of selection operating on gnathopod size during the two se-
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FIG. 3.—A comparison of gnathopod size between males from South Lake and George Pond. Although George Pond males have an overall larger body size, when head length (an index of overall
body size) is used as a covariate South Lake males have a larger gnathopod size than do George Pond
males (ANCOVA, P , 0.001)
lection episodes. Considering first sexual selection arising from differential pairing success,
George Pond males experienced sexual selection for increased gnathopod size, but there
was no evidence that sexual selection was acting on gnathopod size for South Lake males.
Although the large variation surrounding the estimate of sexual selection in South Lake
males makes interpretation of its magnitude questionable, there was no evidence of an
important relationship between gnathopod size and fitness. For the episode of natural selection arising from success in pairing with larger females, George Pond males experienced
selection against larger gnathopod size. In South Lake, selection in the natural selection
episode was near zero and not significant.
The finding in this study that sexual selection acts on residual gnathopod size in the
large-bodied ecotype, but not in the small-bodied ecotype, mirrors conclusions of a previous
study of the two ecotypes in other habitats (Wellborn, 1995b). In the earlier study I found
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significant directional sexual selection on residual gnathopod size for large-bodied ecotype
males in Duck Marsh, but no selection on gnathopods in small-bodied ecotype males in
Duck Lake. The similarity of results in these studies suggests that the presence of sexual
selection on gnathopod size in the large-bodied ecotype, but not in the small-bodied ecotype, may apply broadly to these Hyalella ecotypes in Michigan.
Because selection on gnathopod characters as examined in this study results from the
behavioral process of pair formation, differences in patterns of selection between ecotypes
reflect differences in mating behaviors. These behavioral interactions may be intersexual
(mate choice), intrasexual (male-male competition for mates) or a combination of both.
Although the mechanisms underlying differences in behavioral processes and consequent
selection regimes between ecotypes are not yet known, several possibilities exist. Particularly
intriguing is the possibility that ecotypic differences in mating behaviors may be related to
disparity in predation regime, as is the case in some other taxa (Endler, 1983, 1987; Sakaluk,
1990; Andersson, 1994). Because fish use visual cues to detect prey (Wellborn et al., 1996),
I previously suggested that sexual selection for conspicuous traits, like enlarged gnathopods,
may be constrained by substantial mortality selection against conspicuous characters in the
small-bodied ecotype which occupies habitats with predatory fish (Wellborn, 1995b). Such
constraints would not be present in the fishless habitats of the large-bodied ecotype. This
suggestion seems unlikely, however, in light of the fact that the small-bodied ecotype has
relatively larger gnathopods than the large-bodied ecotype. Disparity in predation regime
may nonetheless still be important for understanding differences in sexual selection between the two ecotypes. Prey species that coexist with predatory fish often exhibit lower
activity levels than prey in fishless habitats (Wellborn et al., 1996), a general pattern that
applies to the two ecotypes in this study (Wellborn, 1993). Predation risk by fish may constrain activity levels in populations of the small-bodied ecotype, and thus constrain behavioral interactions during mating. For example, low activity levels in populations of the smallbodied ecotype may reduce the frequency of intrasexual and intersexual encounters. Reduced encounter rates may constrain or limit male-male aggression and female choosiness
(Real, 1990), leading to low levels of selection in the small-bodied ecotype populations. Low
encounter rates due to inactivity would thus operate analogously to the effects of low population density which may moderate the intensity of selection (Howard and Kluge, 1985;
Zeh, 1987). Differences between ecotypes in selection regime may, of course, be unrelated
to predation or other ecological factors. For example, under Fisherian processes, even small
random differences between populations in initial gene frequencies for trait expression in
males and preference in females may lead to alternative equilibria (Lande, 1981).
Differences between ecotypes in selection regimes may hold implications for understanding diversification of Hyalella ecotypes since differences in mating patterns that lead to
reduced gene flow among populations create a setting that can foster species formation
(West-Eberhard, 1983). Divergence among populations driven by sexual selection may be
an important process in diversification (Lande, 1982; West-Eberhard, 1983; Andersson,
1994) and is even thought to have been important in the extraordinary radiation of species
flocks (Templeton, 1979; Dominey, 1984; Otte, 1989). For Hyalella ecotypes in Michigan
the large-bodied and small-boded forms are largely or wholly reproductively isolated
(McPeek and Wellborn, 1998), and ecotype differences in mating patterns might contribute
to this isolation. In the large-boded ecotype, both large body size (Wellborn, 1995b) and
large residual gnathopod size (Wellborn 1995b; this study) contribute to male mating success, but these traits do not influence male reproductive success in the small-bodied ecotype.
Since these differences in selection reflect differences in intrasexual or intersexual behavioral interactions during mating, they may engender mating incompatibilities between the
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ecotypes. For example, if residual gnathopod size is used by females of the large-bodied
ecotype as a contact signal of male suitability, then males of the small-bodied ecotype may
fail to properly contact the female, and thus be rejected. Also, the generally smaller body
size of the small-bodied ecotype may cause males to be rejected by large-bodied ecotype
females or loose to large-bodied ecotype males in intrasexual contests.
When adjusted for differences in overall body size, the small-bodied ecotype in South
Lake has relatively larger gnathopods than the large-bodied ecotype in George Pond. This
result corresponds to a broader pattern of differences in gnathopod size between the ecotypes in Michigan. This difference does not readily follow from patterns of selection on
gnathopod size in the two ecotypes. In general, we anticipate that the population experiencing greater directional selection on a trait will have the more extreme expression of the
trait. Total directional selection, however, was not significant in either population. In addition, results of this study and the previous study (Wellborn, 1995b) indicate significant
sexual selection for residual gnathopod size in the large-bodied ecotype, but no selection
in the small-bodied ecotype. Together, these results suggest that knowledge of selection due
to paring success and success in pairing with larger females may be inadequate to understand patterns of gnathopod size differences between ecotypes. Perhaps other selective influences, such as survival or resource competition, may strongly influence the evolution of
gnathopod size. Additionally, low trait heritability, or population differences in heritability
may limit any influence of contemporary selection on gnathopod size. Finally, self-limiting
selection may constrain gnathopod size in the large-bodied ecotype since selection favoring
larger residual gnathopod size in the sexual selection episode was reversed in the natural
selection episode.
A potential difficulty in inferring general patterns from results of this study is that selection patterns are documented for only one time period. If selection is variable in time, then
conclusions based on one sample period may not reflect the general pattern of selection
experienced by the populations. Thus, caution is warranted in attempts to explain the
evolution of trait variation from results of this study alone. As noted earlier, however, the
observation in this study that sexual selection acts on residual gnathopod size in the largebodied ecotype, but not in the small-bodied ecotype, confirms conclusions of a previous
study of the two ecotypes in other Michigan habitats (Wellborn, 1995b). The conformity of
results in the two studies suggests that the presence of sexual selection on gnathopod size
in the large-bodied ecotype, but not in the small-bodied ecotype, may apply broadly to these
Hyalella ecotypes in Michigan.
Fluctuating asymmetry in gnathopods does not appear to be important in male mating
success. Gnathopod symmetry of paired males was not different from symmetry of unpaired
males in either population. A rapidly growing number of studies across diverse taxa have
examined the relationship between male mating success and male symmetry, with some
indicating an important role for male symmetry (e.g., Thornhill, 1992; Harvey and Walsh,
1993; Møller, 1994; Simmons, 1995), and others, suggesting that symmetry is not related to
mating success (e.g., Ryan et al., 1995; Dufour and Weatherford, 1998). The mechanism
most often proposed for a relationship between fluctuating asymmetry and mating success
is that females use male symmetry as an indicator of heritable developmental competence
in the face of environmental stresses (Møller, 1990). In large-ecotype Hyalella females do
appear to use gnathopod size for mate selection (Wellborn, 1995b; and this study), but not
gnathopod symmetry. In part, this result may be due to the rather low levels of fluctuating
asymmetry found in gnathopod size. Perhaps gnathopod symmetry is not a sensitive indicator of developmental stability in this taxon, or it becomes important only at times of
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increased environmental stress. Manipulative studies will be required to fully evaluate these
possibilities.
This study demonstrates that large-bodied and small-bodied Hyalella ecotypes in southeast
Michigan differ in patterns of selection acting on gnathopod characters, reflecting concomitant differences in mating behaviors between ecotypes. Although these differences in selection may be related to habitat differences in mortality patterns, the causal mechanisms
are clearly complex and will require additional investigation to elucidate. The combination
of studies like this one that examine the patterns of selection in the field with detailed
mechanistic studies of mating behavior should be particularly informative (Endler, 1986).
In this case it will be especially important to examine mating interactions in detail to determine the extent to which sexual selection arises from female choice or male-male contests and how these differ between the ecotypes. Additionally, it will be important to better
understand the interaction of the roles of body size and gnathopod size in determining
mating success within populations and their consequences for reproductive isolation between the ecotypes. Such comparative studies will help elucidate the evolutionary mechanisms underlying the genesis and maintenance of sexually dimorphic weapons and ornaments.
Acknowledgments.—I thank the University of Michigan for providing access to the E. S. George Reserve and George Pond. I thank R. Cothran and an anonymous reviewer for comments that improved
the manuscript. This research was funded by a research grant from the Hill Fund of the University of
Oklahoma Biological Station and by a Junior Faculty Fellowship from the University of Oklahoma.
LITERATURE CITED
ANDERSSON, M. 1994. Sexual selection. Princeton University Press, Princeton, New Jersey. 597 p.
ARNOLD, S. J. AND M. J. WADE. 1984a. On the measurement of natural and sexual selection: theory.
Evolution, 38:709–719.
AND
. 1984b. On the measurement of natural and sexual selection: applications. Evolution, 38:720–734.
BOROWSKY, B. 1984. The use of males’ gnathopods during precopulation in some gammaridean amphipods. Crustaceana, 47:245–250.
AND R. BOROWSKY. 1987. The reproductive behaviors of the amphipod crustacean Gammarus
palustris (Bousfield) and some insights into the nature of their stimuli. J. Exp. Marine Biol.
Ecol., 107:131–144.
BOUSFIELD, E. L. 1973. Shallow-water gammaridean Amphipoda of New England. Cornell University
Press, Ithaca, New York. 312 p.
COLE, G. A. AND R. L. WATKINS. 1977. Hyalella montezuma, a new species (Crustacea: Amphipoda) from
Montezuma Well, Arizona. Hydrobiologia, 52:175–184.
CONLAN, K. E. 1991. Precopulatory mating behavior and sexual dimorphism in the amphipod Crustacea. Hydrobiologia, 223:255–282.
COOPER, W. E. 1965. Dynamics and production of a natural population of a fresh-water amphipod,
Hyalella azteca. Ecol. Monogr., 35:377–394.
DARWIN, C. 1871. The descent of man and selection in relation to sex. Reprinted in 1981 by Princeton
University Press, Princeton, New Jersey. 475 p.
DE MARCH, B. G. E. 1981. Hyalella azteca (Saussure), p. 61–77. In: S. G. Lawrence (ed.). Manual for
the culture of selected freshwater invertebrates. Canadian Special Publication of Fisheries and
Aquatic Sciences 54.
DICK, J. T. A. AND R. W. ELWOOD. 1989. Assessments and decisions during mate choice in Gammarus
pulex (Amphipoda). Behaviour, 109:235–246.
DOMINEY, W. J. 1984. Effects of sexual selection and life history on speciation: species flocks in African
cichlids and Hawaiian Drosophila, p. 321–249. In: A. E. Echelle and I. Kornfield (eds.). Evolution of fish species flocks. University of Maine at Orono Press.
224
THE AMERICAN MIDLAND NATURALIST
143(1)
DUFOUR, K. W. AND P. J. WEATHERFORD. 1998. Reproductive consequences of bilateral asymmetry for
individual male red-winged balckbirds. Behav. Ecol., 9:232–242.
EDWARDS, T. D. AND B. C. COWELL. 1992. Population dynamics and secondary production of Hyalella
azteca (Amphipoda) in Typha stands of a subtropical Florida lake. J. N. Am. Benthol. Soc., 11:
69–79.
ENDLER, J. A. 1983. Natural and sexual selection on color patterns in poeciliid fishes. Environ. Biol.
Fishes, 9:173–190.
. 1986. Natural selection in the wild. Princeton University Press, Princeton, New Jersey. 336 p.
. 1987. Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae). Anim. Behav., 35:1376–1385.
FAIRBAIRN, D. J. AND R. F. PREZIOSI. 1996. Sexual selection and the evolution of sexual size dimorphism
in the water strider, Aquarius remigis. Evolution, 50:1549–1559.
FRANCE, R. L. 1992. Biogeographical variation in size-specific fecundity of the amphipod Hyalella azteca.
Crustaceana, 62:240–248.
HARTNOLL, R. G. AND S. M. SMITH. 1978. Pair formation and the reproductive cycle in Gammarus
duebenii. J. Nat. Hist., 12:501–511.
HARVEY, I. F. AND K. J. WALSH. 1993. Fluctuating asymmetry and lifetime mating success are correlated
in males of the damselfly Coenagrion puella (Odonata: Coenagrionidae). Ecol. Entomol., 18:
198–202.
HOUDE, A. E. AND J. A. ENDLER. 1990. Correlated evolution of female mating preferences and male
color patterns in the guppy Poecilia reticulata. Science, 248:1405–1408.
HOWARD, R. D. AND A. G. KLUGE. 1985. Proximate mechanisms of sexual selection in woodfrogs. Evolution, 39:260–277.
JONES, R., D. C. CULVER AND T. C. KANE. 1992. Are parallel morphologies of cave organisms the result
of similar selection pressures? Evolution, 46:353–365.
LANDE, R. 1981. Models of speciation by sexual selection on polygenic traits. Proc. Nat. Acad. Sci.,
U.S.A., 78:3721–3725.
. 1982. Rapid origin of sexual isolation and character divergence in a cline. Evolution, 36:213–
223.
AND S. J. ARNOLD. 1983. The measurement of selection on correlated characters. Evolution, 37:
1210–1226.
MATTSON, S. AND T. CEDHAGEN. 1989. Aspects of the behaviour and ecology of Dyopedos monacanthus
(Metzger) and D. porrectus Bate, with comparative notes on Dulichia tuberculata Boeck (Crustacea: Amphipoda: Podoceridae). J. Exp. Marine Biol. Ecol., 127:253–272.
MCPEEK, M. A. AND G. A. WELLBORN. 1998. Genetic variation and reproductive isolation among phenotypically divergent amphipod populations. Limnol. Oceanogr., 43:1162–1169.
MøLLER, A. P. 1990. Fluctuating asymmetry in male sexual ornaments may reliably reveal male quality.
Anim. Behav., 40:1185–1187.
. 1992. Female swallow preference for symmetrical male sexual ornaments. Nature, 357:238–240.
. 1993. Developmental stability, sexual selection and speciation. J. Evol. Biol., 6:493–509.
. 1994. Sexual selection in the barn swallow (Hirundo rustica). IV. Patterns of fluctuating asymmetry and selection against asymmetry. Evolution, 48:658–670.
AND A. POMIANKOWSKI. 1993. Fluctuating asymmetry and sexual selection. Genetica, 89:267–279.
OTTE, D. 1989. Speciation in Hawaiian crickets, p. 482–526. In: D. Otte and J. A. Endler (eds.). Speciation and its consequences. Sinauer, Sunderland, Massachusetts.
POMORY, C. M. 1997. Fluctuating asymmetry: biological relevance or statistical noise? Anim. Behav., 53:
225–227.
REAL, L. 1990. Search theory and mate choice. I. Models of single-sex discrimination. Am. Nat., 136:
376–404.
ROFF, D. A. 1992. The evolution of life histories: theory and analysis. Chapman and Hall, New York.
535 p.
RYAN, M. J., K. M. WARKENTIN, B. E. MCCLELLAND AND W. WILCZYNSKI. 1995. Fluctuating asymmetries
and advertisement call variation in the cricket frog, Acris crepitans. Behav. Ecol., 6:124–131.
2000
WELLBORN: ECOTYPES
OF
HYALELLA
225
SAKALUK, S. K. 1990. Sexual selection and predation: balancing reproductive and survival needs, p. 63–
90. In: D. L. Evans and J. O. Schmidt (eds.). Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany.
SCHLUTER, D. 1988. Estimating the form of natural selection on a quantitative trait. Evolution, 42:849–
861.
SIMMONS, L. W. 1995. Correlates of male quality in the field cricket, Gryllus campestris L.: age, size, and
symmetry determine paring success in field populations. Behav. Ecol., 6:376–381.
STEARNS, S. C. 1992. The evolution of life histories. Oxford University Press, Oxford, UK. 249 p.
STEVENSON, M. M. AND A. E. PEDEN. 1973. Description and ecology of Hyalella texana n. sp. (Crustacea:
Amphipoda) from the Edwards Plateau of Texas. Am. Midl. Nat., 89:426–436.
STRONG, D. R., JR. 1972. Life history variation among populations of an amphipod (Hyalella azteca).
Ecology, 53:1103–1111.
. 1973. Amphipod amplexus, the significance of ecotypic variation. Ecology, 54:1383–1388.
TAYLOR, B. E. AND W. GABRIEL. 1992. To grow or not to grow: optimal resource allocation for Daphnia.
Am. Nat., 139:248–266.
TEMPLETON, A. R. 1979. Once again, why 300 species of Hawaiian Drosophila? Evolution, 33:513–517.
THOMAS, P. E., D. W. BLINN AND P. KEIM. 1997. Genetic and behavioral divergence among desert spring
amphipod populations. Freshwater Biol., 38:137–143.
THORNHILL, R. 1992. Fluctuating asymmetry and the mating system of the Japanese scorpionfly Panorpa
japonica. Anim. Behav., 44:867–879.
WARD, P. I. 1988. Sexual selection, natural selection, and body size in Gammarus pulex (Amphipoda).
Am. Nat., 131:348–359.
WATSON, P. J. AND R. THORNHILL. 1994. Fluctuating asymmetry and sexual selection. Trends Ecol. Evol.,
9:21–25.
WELLBORN, G. A. 1993. Ecology and evolution of life history variation among populations of a freshwater amphipod, Hyalella azteca. Ph.D. Dissertation. University of Michigan, Ann Arbor.
. 1994a. Size-biased predation and the evolution of prey life histories: a comparative study of
freshwater amphipod populations. Ecology, 75:2104–2117.
. 1994b. The functional basis of body size differences between Hyalella (Amphipoda) species. J.
Freshwater Ecol., 9:159–168.
. 1995a. Predator community composition and patterns of variation in life history and morphology among Hyalella (Amphipoda) populations in southeast Michigan. Am. Midl. Nat.,
133:322–332.
. 1995b. Determinants of reproductive success in freshwater amphipod species differing in body
size and life history. Anim. Behav., 50:353–363.
, D. K. SKELLY AND E. E. WERNER. 1996. Mechanisms creating community structure across a
freshwater habitat gradient. Annu. Rev. Ecol. Syst., 27:337–363.
WEN, Y. H. 1993. Sexual dimorphism and mate choice in Hyalella azteca (Amphipoda). Am. Midl. Nat.,
129:153–160.
WEST-EBERHARD, M. J. 1983. Sexual selection, social competition, and speciation. Quart. Rev. Biol., 58:
155–183.
ZEH, D. W. 1987. Aggression, density, and sexual dimorphism in chernetid pseudoscorpions (Arachnida:
Pseudoscorpionida). Evolution, 41:1072–1081.
SUBMITTED 8 JANUARY 1999
ACCEPTED 17 MAY 1999