Integrative and Comparative Biology Advance Access originally published online on June 9, 2008
Integrative and Comparative Biology 2008 48(3):428-436; doi:10.1093/icb/icn058
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The effects of diet on plasma and yolk steroids in lizards (Anolis carolinensis)
*Department of Zoology, Oklahoma State University, Stillwater, OK 74078, USA
Correspondence: 1E-mail: matt.lovern{at}okstate.edu
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Steroids present in egg yolk have been shown to vary as a result of numerous social and environmental influences and to produce both positive and negative phenotypic outcomes in offspring. In the present study, we examined how quality of the diet affects plasma and yolk steroids in the green anole (Anolis carolinensis), a lizard species with genotypic sex determination. We documented the effects of body condition on plasma testosterone (T) and corticosterone (CORT)—steroids with frequently opposing effects—in breeding females and on the T and CORT content of their eggs. We chose to manipulate body condition via diet because resource availability is a relevant, fluctuating variable in the environment to which females can be expected to respond. Field-collected females were housed in the laboratory and kept on either a reduced, standard, or enhanced diet (differing in nutritional quality and/or quantity) for ten weeks. Although females did not differ in body condition at the beginning of the study, we found these diet regimes effective in producing females that differed in condition by the end of the study. Females on diets of enhanced quality were in better condition, produced more, but not heavier, eggs, and had higher plasma T concentrations than did females on a standard diet or one of reduced quality. There was also a significant positive relationship between laying sequence of eggs and yolk T for females on diets of enhanced quality, but not for the females on diets of standard or reduced quality. There were no effects of quality of diet on CORT in plasma or yolk, but yolk T and yolk CORT exhibited a strong positive correlation irrespective of treatment. Females on diets of reduced quality did not differ from females on standard diets either with respect to reproductive output or to endocrine profiles, in spite of being in worse body condition. These results demonstrate that females’ body condition, physiology, and reproductive output can be manipulated by quality of diet, and that changes in deposition of yolk steroids in response to diet may be minimal.
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Introduction |
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It is widely recognized that mothers can influence the fitness of their offspring in a myriad of ways, including via epigenetic processes that affect phenotype largely independent of genotype. Such maternal effects can be defined as influences on offspring phenotype not attributable to offspring genotype, the non-maternal environment, or their combination (Lacey 1998
). Maternal effects may result from, for example, resources acquired during development (or lack thereof), the timing and location of birth or hatching, or behaviors that are transmitted from mother to offspring (Qvarnström and Price 2001). Maternal effects occur in plants (Roach and Wulff 1987) and animals including humans (reviewed by Mousseau and Fox 1998; Kajantie 2006).
The discovery that egg yolk contains steroid hormones revealed a novel and exciting extension of research into maternal effects (Winkler 1993). Steroids are highly conserved across taxa and typically they play central roles in sexual differentiation and development of morphology and behavior (e.g., amphibians: Denver et al. 2002; birds: Balthazart and Adkins-Regan 2002; fishes: Grober and Bass 2002; Bass and Zakon 2005; reptiles: Crews and Moore 2005; Wade 2005; mammals: Cooke et al. 1998; Hines 2002). Prior to the 1990s, the general view had been that oviparous species had limited scope for subtle, plastic maternal effects, particularly in comparison to the substantial opportunity for such effects between mother and embryo in live-bearing organisms. Schwabl (1993), however, documented the presence of yolk steroids in the eggs of canaries and zebra finches, and Adkins-Regan et al. (1995) demonstrated that experimentally elevated transfer of steroids to yolk influences phenotype of the offspring in Japanese quail. Yolk steroids are now known to be common not just in avian taxa, but likely in all oviparous taxa and certainly in those examined thus far, including fishes (McCormick 1998; Manire et al. 2004), turtles (Janzen et al. 1998; Bowden et al. 2001; Elf et al. 2002), alligators (Conley et al. 1997), and lizards (Lovern and Wade 2001; Painter et al. 2002).
The diversity of maternally-derived steroids present in yolk suggests great potential for mothers to bias reproductive investment in ways that can have evolutionary consequences. For example, both social environment and physical condition can cause changes in the sex steroid and glucocorticoid levels of breeding females; specific examples include changes associated with reproductive state, social interactions, and abiotic conditions (Woodley and Moore 1999, 2002; Williams et al. 2005; Navara et al. 2006; Schmaltz et al. 2008). Yolk steroids deposited by females may vary with numerous factors, including laying sequence (Schwabl 1993; Love et al. 2008), the number and proximity of breeding neighbors (Schwabl 1997; Reed and Vleck 2001; Gil et al. 2007), maternal social interactions (Whittingham and Schwabl 2002; Michl et al. 2005; Navara et al. 2006), social status (Müller et al. 2002; Tanvez et al. 2008), simulated predation (Saino et al. 2005), and diet (Verboven et al. 2003; Rutstein et al. 2004; Warner et al. 2007). Such variation strongly suggests a hormonal process for communicating environmental conditions from mother to offspring. Few investigators have measured steroids of both plasma and yolk within the same study. Reported effects of social and physical condition on plasma and yolk steroids remain highly variable across, and sometimes within, species.
As part of our ongoing efforts to understand the factors that influence deposition of yolk steroids, in the present study we examine how body condition, as manipulated by quality of diet, affects steroids in the plasma and yolk of green anoles (Anolis carolinensis). This lizard is well-suited for investigating the effects of maternal steroids on offsprings’ phenotype because we know much about its biology through a long history of field and laboratory investigations (reviewed by Crews 1980; Lovern et al. 2004). Unlike some reptiles in which sex is determined environmentally (e.g., temperature-dependent sex determination), green anoles possess genotypic sex determination (Viets et al. 1994). Females lay single-egg clutches; the left and right ovaries typically alternate in egg production (Smith et al. 1973). This means that processes involved in egg formation—yolking, steroid deposition, ovulation, fertilization, and shelling—are independent for each offspring that is produced and therefore changes in maternal condition have the potential to influence the phenotype of individual offspring. Females exhibit variation in plasma steroids related to reproductive status (Jones et al. 1983; Jenssen et al. 2001; Lovern and Wade 2001) and individual variation in the deposition of yolk steroids (Lovern and Wade 2001). Females also may have the ability to regulate deposition of steroids in yolk independent of the concentrations of circulating steroids in plasma (Lovern and Wade 2003a); regulation of deposition of yolk steroids independent of plasma steroids also has been suggested for leopard geckos (Rhen et al. 2006). No studies of green anoles to date have examined whether social or physical factors might drive variation in plasma and yolk steroids.
Specifically, our objectives in the current study were to document the effects of body condition on plasma testosterone (T) and corticosterone (CORT) in breeding females and on the T and CORT content of their eggs. In this laboratory study, we chose to manipulate body condition via diet because resource availability is a relevant, fluctuating variable in the environment to which breeding females should be expected to respond. Elevated T often has a positive phenotypic effect (e.g., enhanced growth rate, competitiveness, and survival; reviewed by Groothuis et al. 2005) and might be expected when body condition is good, whereas elevated CORT often has a negative effect (e.g., reduced growth rate, altered stress response; Hayward and Wingfield 2004; Saino et al. 2005; Hayward et al. 2006) and might be expected when body condition is poor.
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All procedures described below were conducted in compliance with the Institutional Animal Care and Use Committee at Oklahoma State University (Protocol #AS0415).
Animals and housing
Female green anoles in reproductive condition were purchased from Charles Sullivan Co. (Nashville, TN) in June 2007 and housed in the laboratory under conditions known to maintain reproductive activity (Lovern et al. 2004). Upon receipt, we determined snout-vent length (SVL) to the nearest millimeter and mass to the nearest 0.01 g for each female, after which we toe-clipped them for individual identification and placed them singly into 38 l glass terraria. Because females store sperm (Connor and Crews 1980), they can continue to produce eggs during the breeding season in the absence of males. Each terrarium contained a peat-moss substrate, wooden dowel for perching and basking, water dish, and a 0.75 l nest box containing moistened peat moss. We maintained a 14 : 10 h light : dark cycle using a combination of overhead fluorescent lights and cage-top ultraviolet and incandescent lights. Ambient temperature ranged from 22°C at night to 25–38°C during the day, depending on location in each cage with respect to the incandescent light. Relative humidity averaged 65% (range 46–78%). All terraria were misted daily with water.
Experimental design
Lizards were arbitrarily assigned to one of three diets (n = 9 lizards per group): (1) reduced quality; (2) standard; and (3) enhanced quality. Females in each group were fed crickets (Acheta domesticus) three times per week. Crickets for the group with a diet of reduced quality were maintained on water and cornmeal only, whereas crickets for the lizards on standard and enhanced diets were maintained on water and a mix of carrots, oranges, and dry cricket food (Maintenance Formula, Rep-Cal, Los Gatos, CA). Females with enhanced diets additionally were fed twice per week with waxworms (larvae of the wax moth, Galleria mellonella), which are similar to crickets in size, water content, and protein, but 
350% higher in lipid content (Finke 2002). Supplementation of vitamins and minerals was provided for all groups by dusting crickets on alternate days that they were fed to lizards with a 1 : 1 mix of Herptivite (Rep-Cal, Los Gatos, CA) and Miner-All (Sticky Tongue Farms, Sun City, CA). Crickets were dusted immediately prior to being placed into the lizards’ terraria.
Females were maintained under the conditions described above for 10 weeks. We checked for eggs daily; all eggs were weighed to the nearest milligram and frozen whole at –20°C until analyzed for yolk T and CORT content. At the end of the 10 weeks, we again recorded SVL and mass for each female and blood was collected from the trunk following decapitation. Blood was drawn into capillary tubes coated with heparin and transferred to microcentrifuge tubes. These samples were centrifuged and the resulting plasma fractions were saved at –20°C for determination of circulating T and CORT concentrations.
Radioimmunoassay
Concentrations of T and CORT in the plasma and yolk were measured by radioimmunoassay following extraction and chromatographic separation (Wingfield and Farner 1975; Schwabl 1993). All plasma samples were run in a single assay; all yolk samples were run in a separate, single assay. For plasma, 6–20 µl (recorded to the nearest microliter for each sample) was mixed in 0.5 ml of ddH2O and equilibrated overnight at 4°C with 1000 c.p.m. of 3H-T (NET-370, 70 Ci/mmol) and 3H-CORT (NET-399, 70 Ci/mmol) from PerkinElmer Life Sciences, Inc. (Boston, MA) for individual recovery determinations. For yolk, 20–34 mg (recorded to the nearest mg for each sample) was collected from each frozen egg following separation of the whole yolk from the rest of the egg and thorough mixing with a spatula. These samples were mixed in 1.0 ml of ddH2O and equilibrated with tritiated T and CORT as described for plasma above.
The method of extraction depended on type of sample. Samples of plasma were extracted twice with 2.0 ml diethyl ether, dried under nitrogen gas in a 37°C water bath, and then reconstituted in 0.5 ml of 10% ethyl acetate in isooctane in preparation for chromatography. Samples of yolk were extracted twice with 4.0 ml of a 30 : 70 mixture of petroleum ether : diethyl ether, after which they were dried with nitrogen in a 37°C water bath, reconstituted in 1.0 ml of 95% ethanol, and stored at –20°C overnight. The following day, yolk samples were spun at 2000 rpm for 5 min in a 0°C centrifuge and the supernatant was dried with nitrogen in a 37°C water bath. Samples of yolk were then reconstituted in 0.5 ml of 10% ethyl acetate in isooctane.
For all samples, T and CORT were isolated via column chromatography. Columns consisted of a filter agent : ethylene glycol : propylene glycol upper phase (4 : 1 : 1, m : v : v) and a filter agent : ddH2O (3 : 1, m : v) lower phase. The filter agent (Celpure P300) was purchased from Sigma-Aldrich (St Louis, MO). Neutral lipids and dihydrotestosterone were removed with 2.0 ml isooctane and 1.5 ml 10% ethyl acetate in isooctane, respectively, and discarded. Column fractions containing T and CORT were collected with 2.25 ml 20% and 2.5 ml 52% ethyl acetate in isooctane, respectively. All samples were dried with nitrogen in a 37°C water bath, resuspended in phosphate buffer, and refrigerated at 4°C overnight.
Radioimmunoassays were performed using the appropriate tritiated steroid tracer (see above), antibodies from Research Diagnostics, Inc. for T (T-3003, Flanders, NJ; formerly produced by Wien Labs, Succasunna, NJ) and Sigma-Aldrich for CORT (C8784), and steroid standards from Sigma-Aldrich. The standard curves were run in triplicate and ranged from 0.98 to 250 pg for T and 1.95–500 pg for CORT. Samples were run in duplicate, averaged, and adjusted for individual recovery and initial sample volume. Average recoveries for T and CORT were 49 and 44%, respectively, for plasma and 60 and 42%, respectively, for yolk. Intra-assay CVs, based on four aliquots from a standard pool for each steroid, were 8 and 18% for plasma T and CORT, respectively, and were 4 and 6% for yolk T and CORT, respectively.
Statistical analysis
One female on the enhanced diet never laid an egg over the course of the study and was excluded from all analyses. Female body condition (calculated as the residual of the regression of mass on SVL; Schulte-Hostedde et al. 2005), average egg mass (calculated only for those females that produced at least two eggs), and total output of eggs were each compared across treatment groups using one-way ANOVAs followed by Holm-Sidak post hoc tests when overall P-values were 
0.05. Hormone data also were analyzed using ANOVAs (one-way or general linear models as appropriate) or, when not normally distributed, as was the case for plasma steroids, Kruskal–Wallis tests followed by Dunn's post hoc tests when overall P-values were 0.05. Potential relationships among female condition, egg mass, laying sequence, and plasma and yolk hormones were examined using Spearman rank–order correlation tests.
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Female body condition, egg mass, and output of eggs
Females on the reduced, standard, and enhanced diets did not differ in body condition at the beginning of the study (F2,25 = 0.41, P = 0.67), but they did at the end (F2,25 = 20.21, P < 0.0005). Relative to their initial body condition, females on the reduced diet exhibited a net decrease, females on the standard diet showed no change, and females on the enhanced diet had a net increase in body condition (F2,25 = 13.03, P < 0.0005; Fig. 1A).
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= 0.05.Average egg mass was significantly and positively correlated with initial mass of the female (r = 0.46, P = 0.02); it showed a similar but nonsignificant trend with final mass of the female (r = 0.36, P = 0.07), and did not differ by treatment group (F2,24 = 1.08, P = 0.36; Fig. 1B). A similar result was obtained after excluding from analysis, the first egg from each female—which likely was yolked prior to entering the laboratory (F2,18 = 1.26, P = 0.31). Output of eggs from females on the enhanced diet more than doubled that from females on either the standard or reduced diets (F2,25 = 14.53, P < 0.0005; Fig. 1C). Females on the enhanced diet produced 7.4 ± 0.8 eggs over the course of the 10-week study, whereas females on the standard and reduced diets produced 3.0 ± 0.3 and 3.0 ± 0.7 eggs, respectively.
Concentration of T and CORT in the plasma and yolk
T concentration in the plasma, measured at the end of the study, was significantly higher for females on the enhanced diet than for females on either the standard or reduced diets (H2 = 6.36, P = 0.04; Fig. 2A). No such difference existed in concentration of CORT in the plasma (H2 = 1.24, P = 0.54; Fig. 2B). Neither average concentrations of T (F2,23 = 0.30, P = 0.75; Fig. 2C) nor those of CORT (F2,23 = 0.46, P = 0.64; Fig. 2D) differed among the yolks of eggs produced by females from the different treatment groups. This result held true after excluding the first egg from analysis, both for T (F2,19 = 0.43, P = 0.66) and for CORT (F2,19 = 0.08, P = 0.92), as well as when considering all eggs produced within a treatment group as independent samples, irrespective of female: for T (F2,100 = 1.04, P = 0.36) and CORT (F2,100 = 0.09, P = 0.91).
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Although, we did not detect differences in concentrations of either T or CORT in the yolk when comparing across treatment groups, there were differences among females as well as correlational effects. There was an overall effect of individual female, but not of laying sequence, on the deposition of T in the yolk (female: F23,99 = 1.86, P = 0.02; laying sequence: F9,99 = 0.60, P = 0.80). However, focusing just on the group on enhanced diets, concentration of T in yolk exhibited a significant positive correlation with laying sequence (r = 0.71, P = 0.02). That is, later-laid eggs, on average, tended to have higher concentrations of T in the yolk than did earlier-laid eggs (Fig. 3A). Neither female nor laying sequence affected deposition of CORT in the yolk (female: F23,99 = 0.97, P = 0.51; laying sequence: F9,99 = 0.93, P = 0.50), nor was yolk CORT correlated with laying sequence within the group on an enhanced diet (r = –0.01, P = 0.97; Fig. 3B). For the lizards on standard and reduced diets, no correlation was observed between laying sequence and either T or CORT in the yolk (all P > 0.50). There were no correlations between T and CORT in the plasma (r = –0.06, P = 0.78), plasma T and yolk T (r = 0.18, P = 0.39), plasma T and yolk CORT (r = –0.08, P = 0.70), or plasma CORT and yolk T (r = –0.13, P = 0.56). T and CORT in the yolk were significantly positively related, whether tested for all eggs (r = 0.45, P < 0.005) or by within-female averages (r = 0.67, P < 0.005; Fig. 4).
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Discussion |
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Our study demonstrates that body condition, physiology, and reproductive effort in female green anoles can be manipulated by diet. Females on diets of enhanced quality had better body condition, produced more (but not larger) eggs, and had higher concentrations of T in the plasma than did females on a standard diet or one reduced in quality. These differences had little to no effect on deposition of T or CORT in the yolk, however; females on the three diets of different qualities did not differ in their overall concentrations of T or CORT in the yolk. One potential exception to this pattern was that T (but not CORT) in the yolk positively correlated with laying sequence within the group on the enhanced diet. Furthermore, there was an overall effect of individual female on T (but not CORT) in the yolk, indicating a consistent among-female difference in deposition of T, regardless of treatment. Finally, although plasma and yolk steroids generally were not correlated, consistent with a general ability of female lizards to regulate steroid deposition in yolk (Lovern and Wade 2003
; Rhen et al. 2006), there was a very strong, positive correlation between T and CORT in the yolk.
There are at least two general possibilities why females in the present study did not differ in deposition of steroids in the yolk in spite of dramatic differences that were produced in body condition. One possibility is that adjustment of yolk steroids would confer no selective advantage, particularly when there is the opportunity to adjust reproductive effort. Egg-laying females can adjust effort by increasing either egg mass and/or number of eggs produced. Regardless of treatment, larger females produced larger eggs, consistent with a condition-dependent adjustment of reproductive effort. This relationship between female mass and egg mass is common in green anole populations, although not universal (Michaud and Echternacht 1995). More dramatically, females on the enhanced diet produced more than double the number of eggs than did females on the standard or reduced diets by decreasing their inter-egg interval (23 days between eggs for females given a standard or reduced diet versus 9 days for females on an enhanced diet). The higher concentrations of T in the plasma of females on enhanced diets may have resulted directly from this increased reproductive activity, due to increased vitellogenesis and associated steroidogenesis (Jones et al. 1983; Lovern and Wade 2001). The selective advantage of converting increased energy intake into greater production of offspring (i.e., income breeding; Stearns 1992) is clear and may outweigh any potential benefits of differential allocation of yolk steroids, particularly if there are associated costs. For example, immunosuppression (Navara et al. 2005; Cucco et al. 2008) and elevated metabolic rate independent of growth (Tobler et al. 2007) are potential costs associated with T, and reduced post-hatching development (Saino et al. 2005) and elevated response to stress by the hypothalamic-pituitary-adrenal axis (Hayward and Wingfield 2004) are potential costs associated with CORT.
Alternatively, it is possible that although changes in circulating steroids can respond rapidly to changes in condition, deposition of steroids in the yolk depends on conditions averaged over a longer time. Marshall et al. (2005) found that in female canaries circulating androgens (measured indirectly in fecal samples) but not yolk androgens increased in response to quality of males’ song. They suggested that previous experience, or "physiological inertness," may help to explain the change in steroids in females but not in yolk that they observed. It may also help to explain conflicting results (cf. Gil et al. 2004). Because female green anoles lay eggs beginning about April and continuing through August, and because we received females and began our study in June, our field-collected subjects already had undergone 50% of the breeding season under conditions that were not under our control. Longer-term manipulations may be required to alter steroid levels in yolk. For example, Warner et al. (2007) found that female Jacky dragons that began the breeding season on a diet of high quality produced more eggs and had higher T concentrations in the yolk than did females that began the breeding season on a low-quality diet. Further support for this idea comes from the fact that, in the present study, we found a positive correlation between laying sequence and mean T in the yolk for the females on an enhanced diet. Such an effect would not be equivalent to the pattern seen in many birds i.e., increasing T in the yolk with laying sequence, as first demonstrated by Schwabl (1993), because anoles produce single-egg rather than multi-egg clutches and each follicle is independently yolked (Crews 1980). Rather, this suggests the possibility that females maintained for longer (or initiated sooner in the breeding season) on diets of different qualities may have increased differences in deposition of T in the yolk.
That females on diets of reduced quality in the present study did not differ in endocrine status or reproductive effort from females on the standard diet—in spite of a significant reduction in body condition—suggests that these females were able to physiologically compensate for poor nutrition. We expected to detect an inverse relationship between plasma CORT and body condition as has been demonstrated in numerous studies (Love et al. 2005) and which is consistent with mobilization of energy reserves necessary for continuing egg production. However, no effects of treatment were seen on CORT concentrations in either plasma or yolk; females on enhanced diets did not show reduced CORT, and females on reduced diets did not show elevated CORT. In fact, one of the stronger relationships to emerge from the present study was the positive correlation between CORT and T in the yolk. To date, yolk CORT has not garnered the same attention as has yolk T, although this appears to be changing (Love et al. 2008). Our results demonstrate that CORT is present in the yolks of green anole eggs and is highly related to T content; there is need for further study.
The field of maternal effects via yolk steroids is still young, but it has been provisioned with theoretical as well as empirical nourishment by the dramatic increase in investigators conducting research in this area and the resulting explosion of studies (only partially reviewed above). Growth is strong and maturity will be achieved with advances particularly in the much-needed areas of (1) a mechanistic understanding of the deposition of steroids in the yolk, such as recent contributions from Groothuis and Schwabl (2008) and Paitz and Bowden (2008), and (2) more long-term studies that follow offspring into adulthood to measure effects of yolk steroids on adult endpoints, including reproductive success. Work in our laboratory is continuing to investigate condition-dependent effects on female green anoles that may influence deposition of steroids in the yolk; although effects of diet on yolk steroids may be limited, effects of breeding density and other social factors still require exploration. We are also beginning to investigate how experimentally-manipulated yolk steroids affect physiology, morphology, and behavior of offspring in the short- and long-term. Although it is not necessary that an effect of yolk steroids on phenotype be detectable in adults for it to have increased fitness via specific action during development (e.g., increased likelihood of survival to adulthood), differences in adult phenotype that can be traced to differences in yolk steroids would be additional—and very compelling—evidence for their evolutionary significance.
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We gratefully acknowledge The Society for Integrative and Comparative Biology and the Divisions of Comparative Endocrinology, Animal Behavior, Developmental & Cell Biology, and Ecology & Evolution for supporting the symposium in which this article was originally presented. We also gratefully acknowledge symposium support provided by the National Science Foundation (IOS-0737608 to R.M. Bowden and M.B.L.). We thank Angie Reisch and Chelsea Williams for help with animal care and data collection, and two anonymous reviewers and Harold Heatwole for helpful comments on the manuscript. Research funding was provided by the National Science Foundation (IOS-0641434 to M.B.L.).
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From the symposium "Consequences of Maternally-Derived Yolk Hormones for Offspring: Current Status, Challenges, and Opportunities" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 2–6, 2008, at San Antonio, Texas.
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