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Latitudinal Variation in Life History Reveals a Reproductive Disadvantage in the Texas Horned Lizard (Phrynosoma cornutum)

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Abstract

Geographically widespread species that occupy many thermal environments provide testable models for understanding the evolution of life-history responses to latitude, yet studies that draw range-wide conclusions using descriptive data from populations in the core of a species distribution can overlook meaningful inter-population variation. The phrynosomatid lizard Phrynosoma cornutum spans an extensive latitudinal distribution in North America and has been well-studied in connection with life-history evolution, yet populations occupying the most northern and coldest areas within its range were absent from previous examinations. We tested genus-wide models and challenged species-specific findings on the evolution of the life-history strategy for P. cornutum using populations at the northern edge of its geographic range and comparative material from farther south. Multivariate analyses revealed that egg dimensions decreased with clutch size, suggestive of a previously unrecognized tradeoff between egg size and egg number in this species. Interestingly, reproductive traits of females with shelled eggs did not covary with latitude, yet we found that populations at the highest latitudes typified several traits of the genus and for the species, including a model for Phrynosoma of large clutches and delayed reproduction. A significant deviation from earlier findings is that we detected latitudinal variation in clutch size. This finding, although novel, is unsurprising given the smaller body sizes from northern populations and the positive relationship between clutch size and body size. Intriguing, however, was that the significant reduction in clutch size persisted when female body size was held constant, indicating a reproductive disadvantage to living at higher latitudes. We discuss the possible selective pressures that may have resulted in the diminishing returns on reproductive output at higher latitudes. Our findings highlight the type of insights in the study of life-history evolution that can be gained across Phrynosomatidae from the inclusion of populations representing latitudinal endpoints.
Latitudinal Variation in Life History Reveals a Reproductive Disadvantage in
the Texas Horned Lizard (Phrynosoma cornutum)
Daniel F. Hughes1, Walter E. Meshaka Jr.2, Carl S. Lieb3, and Joseph H. K.
Pechmann4
Running head: Reproductive variation in the Texas Horned Lizard
Key words: clutch size; demography; fecundity; geographic variation; Phrynosomatidae;
Squamata
1Department of Animal Sciences, University of Illinois at Urbana-Champaign, 1207 West
Gregory Drive, Urbana, Illinois 61801; E-mail: dfhughes@illinois.edu. Send reprint requests to
this address.
2Section of Zoology and Botany, State Museum of Pennsylvania, 300 North Street, Harrisburg,
Pennsylvania 17120; E-mail: wmeshaka@pa.gov
3UTEP Biodiversity Collections, Department of Biological Sciences, University of Texas at El
Paso, 500 West University Avenue, El Paso, Texas 79968; E-mail: clieb@utep.edu
4Department of Biology, Western Carolina University, 130 Natural Science Building,
Cullowhee, North Carolina 28723; E-mail: jpechmann@email.wcu.edu
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Geographically widespread species that occupy many thermal environments provide
testable models for understanding the evolution of life-history responses to latitude, yet
studies that draw range-wide conclusions using descriptive data from populations in the
core of a species’ distribution can overlook meaningful inter-population variation. The
phrynosomatid lizard Phrynosoma cornutum spans an extensive latitudinal distribution in
North America and has been well-studied in connection with life-history evolution, yet
populations occupying the most northern and coldest areas within its range were absent
from previous examinations. We tested genus-wide models and challenged species-specific
findings on the evolution of the life-history strategy for P. cornutum using populations at
the northern edge of its geographic range and comparative material from farther south.
Multivariate analyses revealed that egg dimensions decreased with clutch size, suggestive of
a previously unrecognized tradeoff between egg size and egg number in this species.
Interestingly, reproductive traits of females with shelled eggs did not covary with latitude,
yet we found that populations at the highest latitudes typified several traits of the genus
and for the species, including a model for Phrynosoma of large clutches and delayed
reproduction. A significant deviation from earlier findings is that we detected latitudinal
variation in clutch size. This finding, although novel, is unsurprising given the smaller body
sizes from northern populations and the positive relationship between clutch size and body
size. Intriguing, however, was that the significant reduction in clutch size persisted when
female body size was held constant, indicating a reproductive disadvantage to living at
higher latitudes. We discuss the possible selective pressures that may have resulted in the
diminishing returns on reproductive output at higher latitudes. Our findings highlight the
.CC-BY-NC-ND 4.0 International licensepeer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not. http://dx.doi.org/10.1101/364091doi: bioRxiv preprint first posted online Jul. 6, 2018;
type of insights in the study of life-history evolution that can be gained across
Phrynosomatidae from the inclusion of populations representing latitudinal endpoints.
Nearly all animal behaviors are affected by latitudinal variation in climate, including metabolism
(Tsuji, 1988), seasonal activity (Sperry et al., 2010), and predator-prey interactions (Laurila et
al., 2008). These phenomena are intensified in ectotherms because temperature strongly
influences their physiology (Huey, 1982), and many aspects of physiology have implications for
demography (Huey and Berrigan, 2001). For example, growth is slower at higher latitudes from
decreased temperatures that reduce activity and increase dormancy (e.g., Blouin-Demers et al.,
2002; Laugen et al., 2003). Latitudinal variation in ectotherm body size, growth, and mortality
has been well studied (e.g., Adolph and Porter 1993; 1996), however, we know far less about
such variation from direct measures of reproduction. Changes in fecundity can have significant
demographic costs that impact population size and persistence. For example, smaller ectothermic
lizards generally have fewer young (Fitch, 1985). If lizards are smaller at higher latitudes (e.g.,
Ashton and Feldman, 2003), then clutch size is expected to be smaller. Nevertheless, there is a
tradeoff between egg size and clutch size because the offspring number cannot be changed
without changing egg size and thus offspring size and ultimately survival (Sinervo, 1990).
Herein we examine variation in reproductive traits of Texas horned lizards (Phrynosoma
cornutum) from three populations that span most of the species' latitudinal distribution in the
United States.
Body size in lizards is highly variable (Olalla-Tárraga et al., 2006), and patterns often do
not conform to traditional latitudinal explanations for vertebrates (e.g., Bergmann’s Rule
[Angilletta et al., 2004]). Clutch size is tightly linked to body size in lizards (King, 2000), so
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fecundity should vary with latitude. Although body size in lizards is constrained by seasonal
resource acquisition (e.g., Ballinger, 1977; Van Noordwijk and de Jong, 1986), the amount of
time each year that foraging is feasible will decline with increasing latitude. Consequently,
latitudinal patterns in lizard body size covary with several life-history variables, one of which is
clutch size (Angilletta et al., 2004). At higher latitudes, growth is slower as activity seasons
become shorter; a relatively larger body size is usually achieved by prolonged growth and
delayed maturation (Atkinson, 1994). It follows that clutch size should vary widely with latitude,
largely reflecting variation in the active season. Further, latitudinal variation in clutch size should
mirror the variation in body size, and any deviations from this pattern would suggest differential
selective pressures within species populations (Tinkle et al., 1970).
North American horned lizards (Phrynosomatidae: Phrynosoma) have previously been
the subject of many ecological studies in connection to life-history theory (e.g., Ballinger, 1974;
Howard, 1974). Pianka and Parker (1975) conducted a genus-wide examination of horned lizard
species, and described their life-history strategy as belonging to the “delayed reproduction, large
clutch and single brooded” category per Tinkle et al. (1970). Further, Pianka and Parker (1975)
sought to reconcile the heterogeneous life-history strategy in horned lizards (i.e., r-selected for
high fecundity and K-selected for delayed maturity and long lives) with the expectation of higher
juvenile mortality relative to the more homogenous strategies for other phrynosomatid lizards
(e.g., Adolph and Porter, 1993; Pianka, 1970).
Studies of the Texas horned lizard (P. cornutum) have corroborated several genus-wide
patterns and hinted at some geographic trends to its life-history strategy. Across a latitudinal
gradient from Mexico to Colorado, Texas horned lizards exhibit variation in body size with
smaller individuals at northern latitudes (Montgomery et al., 2003), yet not all horned lizards
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exhibit this trend (Pianka and Parker, 1975). The large clutch sizes and delayed maturity among
horned lizards is associated with the production of a single clutch per season (Pianka and Parker,
1975). Clutch frequency in the Texas horned lizard, however, is geographically variable among
populations without demonstrating a regional geographic bias (Ballinger, 1974; Howard, 1974;
Vitt, 1977). A seasonal increase in testis size from May–August is conserved across horned
lizards, and this increase is consistent across longitude in the Texas horned lizard (Ballinger,
1974; Howard, 1974). Delayed reproduction is a genus-wide phenomenon and occurs in Texas
horned lizards from the southwestern United States (Howard, 1974) to Oklahoma (Endriss et al.,
2007). Texas horned lizards exhibit latitudinal variation in clutch size from Texas to Oklahoma
with smaller clutches observed in populations at higher latitudes (Howard, 1974; Vitt, 1977;
Endriss et al., 2007). However, this latitudinal pattern is interpreted without accounting for
established clinal changes in adult body size (i.e., Montgomery et al., 2003).
Museum specimens were the primary source of data for nearly all of the studies on the
Texas horned lizard cited above. In keeping within this well-established framework, we
examined a large series of museum specimens from the northern edge and a southern portion of
the Texas horned lizard’s geographic range to address the following three main questions: (1) are
there geographic patterns in life-history characteristics after controlling for differences in body
size among populations? (2) what is the relationship between egg size and clutch size within and
among populations? (3) are there latitudinal patterns in multivariate life history? Importantly, we
included populations from a higher latitude than previously studied, and we focused on
reproductive traits for which predictability has been lacking in previous investigations.
Essentially, we attempted to use our data—that include the northernmost populations—to resolve
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previously inconsistent life-history findings deduced from narrow geographic sampling for the
Texas horned lizard.
MATERIALS AND METHODS
We examined 213 specimens of the Texas horned lizard (Fig. 1) from the herpetology collections
of the Sternburg Museum (Hays, Kansas) and the University of Texas at El Paso Biodiversity
Collections (El Paso, Texas). The specimens originated from three primary locations: Kansas,
Texas, and New Mexico (Fig. 2). Eighty-seven specimens were collected during 1958–2013
from seven northern counties in Kansas (Ellis, Lincoln, Osborne, Rooks, Russell, Saline, and
Trego). Seventy-three specimens were collected during 1958–2010 from three western counties
in Texas (Culberson, El Paso, and Hudspeth). Forty-five specimens were collected during 1966–
2014 from 10 mostly southern counties in New Mexico (Chaves, Doña Ana, Eddy, Grant,
Hidalgo, Luna, Otero, San Miguel, Sierra, and Socorro). We also examined a smaller sample of
eight specimens that were collected during 1962–1979 from three northern states in Mexico
(Chihuahua, Coahuila, and Durango).
For each specimen, we measured snout-vent length (SVL) with calipers to the nearest 0.1
mm. Lizards were then dissected and sexed. Females were classified as immature or non-
reproductive if the largest ovarian follicle was < 3 mm and not vitellogenic. Females were
assigned as reproductive if they contained shelled eggs or vitellogenic ovarian follicles 3 mm.
Diameters of the largest yolking follicles, and length and width of shelled eggs were measured to
the nearest 0.1 mm. Egg volumes were calculated from the equation for an ellipsoid: v = (4/3)
ab2 (Mayhew, 1963). Clutch volumes were calculated as the product of clutch size and egg
volume. The fraction of length and of mid-testis width/male SVL was used as a measure of
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seasonal male fertility. The ovarian cycle was determined by plotting monthly distribution of the
largest follicle and shelled egg length.
Without direct observations on the number of eggs deposited in each clutch, we estimated
clutch size using counts of shelled eggs and/or vitellogenic ovarian follicles 3 mm. We used a
General Linear Model (GLM) with SVL as a covariate to test if there was a significant difference
between the two clutch measures (shelled eggs and vitellogenic follicles). We found that little
overlap existed in body sizes among populations (Fig. 3), and thus we tested whether the slopes
of the regression lines between SVL and clutch size differed among populations or by clutch
measure by testing for interaction effects among these variables using a GLM. Because SVL is
linearly related to clutch size in Texas horned lizards (Ballinger, 1974; Howard, 1974) and to
avoid potential problems with the use of ratios in statistics (Packard and Boardman, 1999), all
measurements were analyzed in an analysis of covariance (ANCOVA) with SVL as a covariate
to remove the effect of body size in our comparisons of life-history variables among populations.
We explored multivariate divergence of the three primary populations with principal
component analysis (PCA). To avoid weighting variables by their variance, the PCA was
performed using a correlation matrix calculated from population means of five life-history
characters (clutch size, egg length, egg width, egg volume, and clutch volume). We restricted
this analysis to females with shelled eggs only. One female specimen from New Mexico with
shelled eggs was excluded because of the eggs were rounded. Measurements were natural-log
transformed and size corrected using SVL as a covariate because all five measurements were
positively correlated with body size. The residuals were saved and included as input for PCA.
We used standardized guidelines to determine that our data met the assumptions (e.g., normality)
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of PCA (McGarigal et al., 2000). All statistical analyses were conducted in Minitab v. 17
(Minitab Statistical Software, State College, Pennsylvania, USA).
RESULTS
Testicular cycle.—Testis length and width varied seasonally in all three populations (Fig. 4A–
C). Among males in Kansas and Texas, testes were largest in April and smallest in July (Fig 4.
A, B). In New Mexico, testes reached a maximum size in June and rapidly decreased in size
thereafter, with the smallest sizes evident in July (Fig. 4C).
Nesting season.—The nesting season was short (ca. 2–3 months) in all three populations, and
some overlap was evident among them (Fig. 4D–F). In Kansas, shelled eggs were present in
females during May–June (Fig. 4D). In Texas, ovigerous females were present also for two
months, beginning one month later (June–July) (Fig. 4E). The longest nesting season (May–July)
was detected in New Mexico, which subsumed the combined nesting season of the other two
regions (Fig. 4F).
Clutch size.—Because we had two measures of clutch size (shelled eggs and yolked ovarian
follicles) from three discrete populations (Kansas, Texas, and New Mexico), we first tested for
interactions between various variables associated to know if we could reliably compare clutch
sizes among populations. The interaction between population X clutch measure was not
significant (F2,37 = 0.51, P = 0.607), and the interaction among population X clutch measure X
body size was also not significant (F2,37 = 0.46, P = 0.637). As a result, we felt that the intercept
of these regression lines could be validly compared because the slopes are essentially parallel
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(Fig. 2). Further, we found that there was no difference in our clutch size estimates between the
two measures of clutch size among the three populations (F1,37 = 3.41, P = 0.074) and thus we
pooled these values for the following analyses involving clutch sizes. After removing the effects
of maternal body size, we found that there was a significant effect of source population on clutch
size, with the smallest mean clutch size found in Kansas, intermediate in New Mexico, and
largest in Texas (F2,37 = 3.62, P = 0.039) (Table 1). Size-corrected analyses detected no
significant difference among populations in mean clutch volume (F2,15 = 1.2, P = 0.336) (Table
1).
Shelled egg size.—Size-corrected analyses detected no significant differences among
populations in the means of egg length (F2,15 = 0.1, P = 0.903), egg width (F2,15 = 1.16, P =
0.346), or egg volume (F2,15 = 0.73, P = 0.503) (Table 1). Because egg length (R2 = 61.3%, F1,15
= 23.79, P < 0.001), egg width (R2 = 85.2%, F1,15 = 87.03, P < 0.001), and egg volume (R2 =
81.8%, F1,15 = 63.11, P < 0.001) were positively correlated with SVL, we removed the effects of
body size by calculating residual scores from the separate regressions of each metric (and clutch
size) on maternal SVL. Using the resulting residuals in separate regression analyses revealed a
negative relationship between clutch size and egg sizes—there was an overall decrease in
residual egg length, egg width, and egg volume with increasing residual clutch size (Fig. 5A–C).
Clutch frequency.—We only detected luteal scars associated with expended oviductal eggs, and
concurrent ovarian follicles measured 2–3 mm. We found a single female collected in June from
Saline County, Kansas, that had 29 shelled eggs and 25 yolked ovarian follicles > 3 mm,
suggesting that this individual had the potential to lay a second clutch that year given acceptable
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energetic or environmental conditions. These findings suggest that females from these three sites
typically produce a single clutch annually, however, we could not rule out multiple clutch
production in some individuals.
Monthly activity.—We detected activity based on pooled capture dates across locations. We
found that the activity in the Texas horned lizard ranged from four to seven months. Months of
capture were longest in Texas (March–October), followed by Kansas (April–October), New
Mexico (April–September), and Mexico (June–October). For three of the locations, captures
ended in October.
Age at sexual maturity.—The smallest juvenile we examined measured 22.6 mm SVL from Ellis
County, Kansas, captured on 14 September 1963. Body-size cohorts were apparent in monthly
distributions of body sizes for Kansas (Fig. 4G). We presume May and June eggs to have
hatched within two months of oviposition. We do not know how much growth would have
occurred from July and August hatching to our first juvenile cohort in September (22.6–29.2
mm). However, little growth appeared between fall and the following spring capture (26.4 mm).
Fastest growth would have resulted in sexual maturity of males as early 12–13 months of age.
Females and all other males would have reached sexual maturity during their second spring of
life at an age of about 21–22 months of age (Fig. 4G). Too few data were available for the
remaining three locations to estimate growth rates from monthly distributions of body size (Fig
4. H–I).
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Body size at sexual maturity.—Body sizes of adult males followed a latitudinal trend of
increasing size from north to south with respect to minimum, maximum, and mean values (Fig.
6; Table 1). Mean male SVL in Kansas was significantly smaller than in New Mexico, Texas,
and Mexico (F3,105 = 161.19, P < 0.001). Likewise, body sizes of adult females followed a
geographic trend of increasing size from north to south with respect to minimum and mean
values. Mean female SVL in Kansas was significantly smaller than in New Mexico, Texas, and
Mexico (F3,79 = 54.63, P < 0.001) (Fig. 6; Table 1).
Sexual dimorphism in adult body size.—Sample sizes from three sites were large enough to test
for differences in mean adult body sizes between the sexes. Mean body size of adult males was
found to be significantly smaller than that of adult females from Kansas (t = -7.77, df = 63, P <
0.001), New Mexico (t = -3.06, df = 42, P = 0.004), and Texas (t = -5.76, df = 68, P < 0.001)
(Table 1).
Trends in multivariate life history.—The pattern of differentiation among populations and
latitudinal influences are presented in Fig. 7A–B. Relationships among populations were
adequately represented in two dimensions judging by the magnitude of their respective
eigenvalues; the first two dimensions explained 95% of the total variance (Fig. 7A). Three of the
five variables loaded similarly on PC1, which overall described 65% of the variation in the data
(Table 2). The first eigenvalue showed a moderate negative loading on clutch volume and clutch
size, and moderate positive loadings on egg length, egg width, and egg volume. For PC2, which
explained 30% of the variance, the second eigenvalue had the highest positive loading for clutch
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volume and relatively high for clutch size, and low positive loadings for egg width, egg volume,
and egg length (Table 2).
The majority of the variation in our data was described by PC1 and PC2 which were
easily interpreted. Thus, we used the scores for these axes to test the hypothesis that latitudinal
clines are derived from a co-adaptation of life-history traits. The scores on the first principal
component showed a non-significant relationship with latitude (R2 = 2.5%, F1,15 = 0.36, P =
0.556) (Fig. 7B). The second principal component also exhibited a non-significant relationship
with latitude (R2 = 4.7%, F1,15 = 0.69, P = 0.421). We did not find support for the hypothesis that
the clutch measurements we included in this analysis covary with latitude.
DISCUSSION
The life-history strategy of Texas horned lizards seems to have remained highly conserved as the
species expanded its range northward after the last glaciation. The nesting season in Kansas is
delayed by just a month compared to Texas, and in New Mexico the season spans from the
beginning of that in Texas to the end of that in Kansas. The male gonadal cycle of maximal size
in spring, minimal size in summer, and recrudescence in fall is generally consistent from 39ºN to
25ºN. Further, the overall pattern of monthly activity is nearly identical from Mexico to Kansas,
and a two-year interval to reach maturity is also maintained across latitude. The similarity among
populations is even more remarkable given the fact that drastic climatic differences exist among
locations and our findings of adult body size differences. We did find pronounced differences in
clutch sizes among Texas horned lizards, however. We detected latitudinal signatures in body
sizes and consequently clutch sizes, but did not detect a strong influence of latitude in
multivariate life history among populations. We will first discuss reasons as to why seasonal
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activity patterns and age at maturity are so conserved in Texas horned lizards and then we
address latitudinal variation in life history and the implications of our results.
The nesting season of Texas horned lizards, for the most part, is restricted to a few
summer months: May–June in Texas (Pianka and Parker, 1975) and Kansas (this study), May–
July in southern Kansas (Gilver, 1922), central Texas (Ballinger, 1974), and southern New
Mexico (this study), June–July in western Texas (this study), and June–August in the
southwestern United States (Howard, 1974). Our results corroborate the evidence for a relatively
short nesting season throughout its range in the United States, and, as did Gilver (1922) in
southern Kansas, we found that the northernmost population exhibits a strikingly similar range.
Our expectation that nesting activity patterns would vary latitudinally was based on temperature
being of significant importance to ectotherm physiology (Huey, 1982). However, monthly
activity and the nesting season seemed to exhibit only minor shifts in relation to temperature
changes. Nesting and activity do not appear to simply be explained by temperature, at least in
Kansas. Thus, some other factor that varies seasonally must underlie these behaviors. Lizards
behaviorally thermoregulate to maintain activity levels necessary to meet seasonal needs such as
reproduction (e.g., Adolph, 1990). Mating in the Texas horned lizard occurs largely in the spring
and can extend into early summer: April–May in Kansas, April–June in Texas, and June–July in
New Mexico. Increased activity during the mating season suggests that, following mating, the
lizards become less active than thermal conditions would allow. This pattern presumably
represents a tradeoff between activity and survival.
Characterized as delayed breeders, several species of horned lizards reach sexual maturity
at two years of age (Pianka and Parker, 1975), including the Texas horned lizard (Ballinger,
1974; Howard, 1974; Endriss et al., 2007). Using our smallest individual (22.6 mm SVL), a two
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year-estimate of age at sexual maturity in northern Kansas does not differ from that of other
studies, which is even more remarkable in light of marked differences in body sizes among
populations. Juveniles and hatchling Texas horned lizards typically are found in the Fall across
its range: August in central Texas (Ballinger, 1974), June–October from several sites along the
US–Mexico border (Howard, 1974), late-July–August in central Oklahoma (Endriss et al., 2007),
and late-August–September in Colorado (Montgomery and Mackessy, 2003). We do not know if
all of the cohort of young individuals taken in September from northern Kansas represent
hatchlings or a mix of both hatchlings and individuals hatched earlier in the season. The latter
seems likely; based on likely hatching months, the earliest maturing individuals in northern
Kansas would still not breed for the first time until nine months later. Our findings are
inconsistent with Adolph and Porter’s (1996) model that populations from colder environments
mature at a later age and at a larger size than populations in warmer areas (e.g., Wapstra et al.,
2001). Alternatively, Texas horned lizards occupying colder, northern habitats reached sexual
maturity at the same age as their counterparts from warmer, southern areas but at smaller sizes.
Several other phrynosomatid lizards exhibit this same general trend (e.g., Parker and Pianka,
1975; Mathies and Andrews 1995), as does an Australian skink (Forsman and Shine, 1995).
From Colorado to Mexico, adult body sizes in Texas horned lizards of both sexes
decreased from south to north in a latitudinal cline (Montgomery et al., 2003). We found a
similar pattern of decreasing adult body size with increasing latitude. A latitudinal trend in body
size is often attributed to differences in climate decreasing activity (Angilletta et al., 2004),
environmental differences in food availability (Ashmole, 1963), or even day length (Rose and
Lyon, 2013). Our results suggest that to maintain the highly conserved two-year constraint to
reach sexual maturity, adult body sizes exhibit marked latitudinal differences dependent upon
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environmental variables. Indeed, we found that the most northern population and those in the
middle of its range exhibit the same pattern of delayed maturity, but maturity was reached at a
smaller size to compensate for reduced activity and likely reduced growth at high latitudes.
A significant departure in the life history of the Texas horned lizard was found in the
clutch characteristics in our samples. Across its geographic range, the Texas horned lizard
produces large clutches (Givler, 1922; Ballinger, 1974; Howard, 1974; Pianka and Parker, 1975;
Vitt, 1977; Endriss et al., 2007), and our data corroborate that finding. A significant difference,
however, exists among our sites, such that females from the northernmost site produced the
smallest clutches. This finding also held true when female body size was held constant among
our sites. Thus, selection seems to work against fecundity in Texas horned lizards at the northern
edge of their range, placing them at a unique disadvantage of diminishing returns in energy
investment to reproductive output. Ballinger (1974) found no evidence of geographic variation in
clutch size, either latitudinally in Texas or longitudinally along the US–Mexico borderlands. The
absence of a latitudinal trend in his study is understandable. We suspect that Ballinger’s (1974)
finding is best explained by sampling of the species within the center of its geographic range,
where clutch sizes are all similarly large.
Egg size in Texas horned lizards has not been examined previously with respect to clutch
size. With female SVL held constant, we found that the relationships between clutch size and
three measures of egg size were negative. The tradeoff between offspring number and egg size is
mediated by a fecundity advantage of producing small offspring balanced against the survival
advantage of large offspring. Although not measured for the Texas horned lizard, egg size is
generally correlated with offspring size in lizards (Sinervo, 1990; Forsman and Shine, 1995). We
found strong support for the prediction that clutch size is inversely related to egg size (i.e.,
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offspring size) (Stewart, 1979). The amount of energy allocated to reproduction by females is
divided between clutch size and egg size, and thus as clutch size increases egg size decreases. In
fact, many oviparous squamates exhibit this tradeoff between the number and the size of
offspring (e.g., Ford and Seigel, 1989).
Although a single clutch per year is produced in central Texas (Ballinger, 1974) and
eastern Arizona (Vitt, 1977), multiple annual clutch production appears to more common than
previously thought in Texas horned lizards. We could not entirely rule out the possibility of
multiple clutches from our Texas and New Mexico samples and we found one female in Kansas
that had shelled eggs and yolked ovarian follicles (> 3 mm) concurrently. Howard (1974) found
evidence of double clutching in a sample of 21 females from four populations ranging
longitudinally along the US–Mexico border. Wolf (2012) found that 6 of 9 radio-tracked females
from central Oklahoma deposited two clutches in 2011. Further, Wolf et al. (2014) showed that
nearly half of the females from central Oklahoma and about a third from south Texas produced
two clutches annually. There remains the possibility that triple-clutching occurs in southern
Texas populations (Burrow, 2000) based on observations of continual nesting throughout the
active season (Wolf, 2012; Wolf et al., 2014). Texas horned lizards exhibit a slightly longer
season of activity in south Texas (February–December with most activity April–August [Moeller
et al., 2005]), which may contribute to additional egg-laying bouts. Sufficient time for the
production of multiple clutches is feasible in south Texas. However, this interval does not
explain multiple clutch production in Oklahoma. Mechanisms underlying multiple clutch
production in northern populations of the Texas horned lizard are unclear, and may be related to
a combination of favorable environmental triggers such as warmer temperatures and increased
food intake. The effects of these variables on horned lizard fecundity are worth exploring.
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From their respective study sites, Ballinger (1974) considered the Texas horned lizard to
be K-selected for most traits (e.g., delayed maturity), yet r-selected for clutch size and juvenile
survivorship, and Howard (1974) concluded that the species was also K-selected for late-
maturity and r-selected to produce multiple large clutches annually. Reproductive characteristics,
age at sexual maturity, and adult body sizes of the Texas horned lizard in our study included
specimens from sites much farther north than examined by Howard (1974) and Ballinger (1974).
Those specimens provided the material necessary to test the extent to which earlier findings
concerning life history traits were applicable to this species and the genus. Our analyses show
extreme conservatism in many life-history characteristics across its range, yet we detected a
considerable extent of geographic variation in several direct measures of fecundity.
Conclusions.—The Texas horned lizard is a geographically widespread species (Price, 1990)
whose categorization in life-history theory has been based on populations largely exclusive of
the most northern and southern latitudes. Interestingly, even with samples from the northern edge
of its range included, we found that the species generally conformed to Ballinger’s (1974)
findings in Texas populations and Pianka and Parker’s (1975) genus-wide model. However, we
found the smallest clutch sizes from populations in the northernmost locations and, importantly,
a reduction in clutch size was not a simple consequence of body size variation among
populations. Significant differences were still evident after we statistically controlled for the
effects of maternal body size. Geographic variation in body size varies among many species of
reptiles, and directions or absences of latitudinal signatures in this trait vary among them (e.g.,
Meshaka and Layne, 2015). In Texas horned lizards, the reproductive costs associated with
living in northern Kansas is the most extreme (Shine, 1992). Unlike some of the Texas
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populations comprised of very large females that produce a single large clutch or multiple
clutches each year, those in Kansas are restricted to a significantly smaller clutch with a
potentially reduced likelihood of multiple clutch production. It remains to be tested as to what
the latitudinal endpoint is for this ostensibly disadvantageous life-history response in the Texas
horned lizard.
We are intrigued by the reduction in clutch size apart from female body size in northern
Kansas because these populations persist at a distinct disadvantage with respect to fecundity.
Further, we wonder what selective pressures drive the lower fecundity in the northern edge of its
range, and we consider that this species at that latitude may be subjected to reduced opportunities
for not only foraging on a bereft prey base and but also for photosynthesizing vitamin D3, a
hormone necessary for calcium metabolism (Holick, 2010). Whitford and Bryant (1979)
demonstrated irrefutably that Texas horned lizards are food limited and exhibit a pronounced
preference for harvester ants (Pogonomyrmex spp.). Although the extent of this dietary
dependence is subject to variation (e.g., Milne and Milne, 1950; Ramakrishnan et al., 2018),
harvester ant densities and colony sizes are geographically variable (MacMahon et al., 2000;
Warburg et al., 2017). In fact, harvester ant densities were found to be far greater at a central
Texas site compared to a southern New Mexico site (Whiting et al., 1993). Also, the diversity of
New World ants follows a latitudinal cline with fewer species at higher latitudes (Kaspari et al.,
2003), and this pattern is consistent for seed-eating ants across the American Southwest
(Davidson, 1977). At northern latitudes, lizard life histories are sensitive to both reductions in
nutritional energy intake (Ballinger, 1977) and the availability of suitable thermal microclimates
as they relate to the endogenous production of vitamin D3 by exposure to ultraviolet-B (290–315
nm)—a major component of nutritional quality for the Texas horned lizard (Ferguson et al.,
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2015) and crucial for lizard reproduction (Ferguson et al., 1996). The apparent disadvantage in
fecundity we observed in northern populations of the Texas horned lizard may be related to
compromised opportunities for vitamin D3 production from reduced aboveground activity. We
suggest that not only a reduction in the extent of its preferred prey base—both diversity and
abundance—but also decreased opportunities to produce vitamin D3 are linked to the diminished
fecundity in Texas horned lizard populations at northern latitudes.
ACKNOWLEDGMENTS
First and foremost, we dedicate this work to Royce E. Ballinger and the late C. Wayne Howard
in recognition for their excellent contributions to this topic over 40 years ago. This study would
not have been possible without the personal and professional kindnesses of Curtis J. Schmidt,
Curator of vertebrate collections of the Sternberg Museum and we extend our most sincere
gratitude to him.
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Figure legends
Fig. 1. Texas horned lizards (Phrynosoma cornutum) from Doña Ana County, New Mexico. (A)
Gravid female, (B) male and female in coitus, and (C) facial rubbing immediately post coitus.
Fig. 2. Map showing the populations of the Texas horned lizard (Phrynosoma cornutum) we
examined for life histories: Kansas (1), Texas (2), New Mexico (3), and Mexico (4). The species’
geographic distribution (shaded area) was modified from Hammerson (2007).
Fig. 3. Clutch size regressed against body size for three populations of the Texas horned lizard
(Phrynosoma cornutum). Filled symbols represent shelled eggs and open symbols vitellogenic
ovarian follicles. The prediction interval is denoted by a dark-grey tightly spaced dashed line and
the 95% confidence interval is denoted by a light-grey loosely spaced dashed line.
Fig. 4. Monthly distribution of three life-history traits in the Texas horned lizard (Phrynosoma
cornutum) from three populations. Top row: Testis length and width as a fraction of male snout-
vent length (SVL) for (A) Kansas (n = 39), (B) Texas (n = 38), and (C) New Mexico (n = 17).
Filled circles represent testis length/SVL and open circles testis width/SVL. Middle row: Largest
ovarian follicle diameters and shelled egg lengths for (D) Kansas (n= 26), (E) Texas (n = 27),
and (F) New Mexico (n = 25) New Mexico. Filled circles represent shelled eggs and open circles
ovarian follicles. Bottom row: Body size (SVL) for (G) Kansas (39 males, 25 females, 22
juveniles), (H) Texas (42 males, 26 females, 3 juveniles), and (I) New Mexico (19 males, 25
females, 1 juvenile).
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Fig. 5. Tradeoff between egg size and clutch size after statistically removing the effects of
maternal body size in three populations of the Texas horned lizard (Phrynosoma cornutum). (A)
Residuals for egg length plotted against residual clutch size; (B) residuals for egg width plotted
against residual clutch size; and (C) residuals for egg volume plotted against residual clutch size.
The prediction interval is denoted by a dark-grey tightly spaced dashed line and the 95%
confidence interval is denoted by a light-grey loosely spaced dashed line.
Fig. 6. Body size regressed against latitude in four populations of the Texas horned lizard
(Phrynosoma cornutum). The prediction interval is denoted by a dark-grey tightly spaced dashed
line and the 95% confidence interval is denoted by a light-grey loosely spaced dashed line. Filled
symbols represent males and open symbols females.
Fig. 7. Multivariate life-history divergence for three populations of the Texas horned lizard
(Phrynosoma cornutum). (A) Scatter plot of the first two principal components extracted from
five life-history variables that were corrected for maternal body size. (B) Scores of principal
components 1 (see Table 2 for loadings) plotted against latitude (y = 3.061 – 0.089x, R2 = 2.5%,
P = 0.556).
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Table 1. Summary of life-history characters for populations of the Texas horned lizard
(Phrynosoma cornutum). Means ± standard deviation are followed by ranges and samples sizes
for body size, clutch size, egg length, egg width, egg volume, and clutch volume.
Variable Kansas Texas New Mexico Mexico
Male SVL (mm) 60.5 ± 4.3
50.4–68
39
87.3 ± 5.3
73.8–99.2
43
83.6 ± 9.1
69.2–100.4
19
90 ± 6.4
83.5–98.1
5
Female SVL (mm) 70.8 ± 6.4
61.6–86.1
26
96.8 ± 8.5
79.1–113.3
27
92 ± 9.1
73.2–107.5
25
103.9 ± 5.9
99.8–108.1
2
Juvenile SVL (mm) 36.6 ± 11.9
22.6–59.3
22
53 ± 10.7
40.7–59.6
3
39.6
1 46.1
1
Clutch Size (pooled) 20.6 ± 6
12–35
15
28.2 ± 9.7
14–44
13
25 ± 7.2
15–40
10 -
Yolked Ovarian Follicles 21.4 ± 6
14–35
10
28.7 ± 11.8
15–44
6
25.8 ± 9
18–40
5 -
Shelled Eggs 19 ± 6.3
12–29
5
27.7 ± 8.4
14–41
7
24.2 ± 5.8
15–31
5 -
Egg Length (mm) 12.3 ± 1.1
9.8–14.6
96
14.5 ± 0.9
11.8–16.2
188
13.8 ± 1.5
10.9–16.8
115 -
Egg Width (mm) 8.2 ± 0.8
6.7–9.9
96
10.3 ± 0.7
8.2–12
188
9.9 ± 1.3
7–12
89 -
Egg Volume (cm3) 440.3 ± 105.9
256.2–682.5
96
810.9 ± 120.6
470.5–1,076.8
188
755.4 ± 243.6
297.6–1,226.7
89 -
Clutch Volume (cm3) 8,365.9 ± 4,156.5
3,675.1–14,931
5
22,240.6 ± 8,289.9
9,715.8–35,964.7
7
16,808.3 ± 7,205.5
10,472.4–25,450.8
4 -
Female SVL with Shelled
Eggs
73.9 ± 8.9
62.2–86.1
5
102 ± 4.4
97.1–107.5
7
95.9 ± 7.9
84.3–104.6
5 -
Female SVL with Yolked
Ovarian Follicles
68.3 ± 5.9
61.6–77.6
10
98.1 ± 2.9
94.3–101.6
6
96.4 ± 5.1
89.8–103.7
5 -
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Table 2. Principal components analysis comparing populations of the Texas horned lizard
(Phrynosoma cornutum) with five life-history characters regressed against snout–vent length
(SVL). Loadings, eigenvalues, variance, and cumulative variance are shown for the first two
principal components. Values in bold represent the variables with the highest loadings.
Variable PC1 PC2
1 Clutch Size/SVL – 0.442 0.486
2 Egg Length/SVL 0.496 0.172
3 Egg Width/SVL 0.486 0.318
4 Egg Volume/SVL 0.519 0.283
5 Clutch Volume/SVL – 0.231 0.743
Eigenvalue 3.259 1.483
Proportion (variance) 0.65 0.30
Cumulative (variance) 0.65 0.95
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.CC-BY-NC-ND 4.0 International licensepeer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not. http://dx.doi.org/10.1101/364091doi: bioRxiv preprint first posted online Jul. 6, 2018;
.CC-BY-NC-ND 4.0 International licensepeer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not. http://dx.doi.org/10.1101/364091doi: bioRxiv preprint first posted online Jul. 6, 2018;
.CC-BY-NC-ND 4.0 International licensepeer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not. http://dx.doi.org/10.1101/364091doi: bioRxiv preprint first posted online Jul. 6, 2018;
.CC-BY-NC-ND 4.0 International licensepeer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not. http://dx.doi.org/10.1101/364091doi: bioRxiv preprint first posted online Jul. 6, 2018;
.CC-BY-NC-ND 4.0 International licensepeer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not. http://dx.doi.org/10.1101/364091doi: bioRxiv preprint first posted online Jul. 6, 2018;
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