Behavioral Ecology Advance Access originally published online on November 21, 2007
Behavioral Ecology 2008 19(1):208-216; doi:10.1093/beheco/arm124
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Are there benefits to being born asynchronously: an experimental test in a social lizard
School of Zoology, Private Bag 05, University of Tasmania, Tasmania 7001, Australia
Address correspondence to E. Wapstra. E-mail: erik.wapstra{at}utas.edu.au.
Received 8 June 2007; revised 22 October 2007; accepted 24 October 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Hatching asynchrony, or processes analogous to hatching asynchrony (i.e., birthing asynchrony), has now been identified in a number of nonavian taxa. These systems are of importance because, unlike birds, they allow us to decouple hatching asynchrony hypotheses related to adaptive hatching patterns, which suggest that it confers a fitness benefit to either the parent or offspring, from those that focus on the onset of parental incubation. However, to date research on these systems has remained descriptive, solely documenting the extent of asynchronous hatching/birthing. Here we provide the first experimental test of the potential adaptive nature of hatching/birthing asynchrony outside avian systems. Using the birth hormone arginine vasotocin, we manipulated the birthing (a)synchrony of females in a population of the lizard Egernia whitii and examined the effect on offspring growth and survival. We show offspring from asynchronous treatments suffered increased mortality but benefited from increased mass at 6 weeks compared with offspring in synchronous treatments. Differences in mortality and size between treatments were driven by offspring mass at birth, and the development of a greater mass hierarchy within asynchronous compared with synchronous litters. This resulted in the smaller offspring suffering both an increased risk of mortality and decreased growth. Despite this, the mechanism by which these patterns are produced remains unclear, as we found no link between birth order and mortality, size, or any factors that affected either of these.
Key words: Egernia whitii, hatching asynchrony, maternal effects, sibling rivalry, sociality.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Hatching asynchrony in birds describes the time span between the hatching of the first and last egg (Stenning 1996
), usually resulting in the establishment of a size hierarchy within the brood, with the last chick often dying at some stage before fledging. The majority of hypotheses aimed at explaining hatching asynchrony consider this nestling size hierarchy produced by asynchronous hatching to be adaptive (Stoleson and Beissinger 1995). That is, hatching asynchrony can be explained as a mechanism to increase either parental fitness (e.g., peak load reduction hypothesis—Mock and Schwagmeyer 1991; Hebert and McNeil 1999, dietary diversity hypothesis—Magrath 1990, larder hypothesis—Alexander 1974), or offspring fitness (e.g., brood reduction hypothesis—Lack 1954, hurry up hypothesis—Hussell 1972, insurance hypothesis—Forbes et al. 1997, sibling rivalry hypothesis—Hahn 1981, sex ratio manipulation hypothesis—Slagsvold 1990). However, despite the large body of work undertaken to test adaptive hypotheses, none have found unequivocal support and in many cases we are unsure as to whether an adaptive explanation for hatching asynchrony exists (Stoleson and Beissinger 1995). One of the major reasons for this is that birds are physiologically constrained to ovulate eggs asynchronously and do not have the capacity for retaining eggs in utero, thus eggs must also be laid asynchronously (Blackburn and Evans 1986; Norris 1997). Therefore, selective pressures to initiate incubation at some stage prior to all eggs being laid (e.g., limited breeding opportunities hypothesis—Beissinger and Waltman 1991, egg viability hypotheses—Arnold et al. 1987, egg protection hypothesis—Beissinger et al. 1998, brood parasitism hypothesis—Kendra et al. 1988) could generate hatching asynchrony in the absence of any benefits of a size hierarchy per se (reviewed by Magrath 1990; Stoleson and Beissinger 1995). Separating out the adaptive hypotheses versus those that focus on the onset of incubation remains one of the central challenges to our understanding of hatching asynchrony.
The problems associated with understanding hatching asynchrony, and specifically the uncoupling of these 2 sets of hypotheses, have long been restricted to the avian literature. However, recent research has shown that hatching asynchrony is more widespread than previously thought. Hatching asynchrony has now been identified in a number of invertebrate systems (Cryptocercus punctulatus, Nalepa 1988; Nicrophorus vespilloides, Muller and Eggert 1990; Smiseth et al. 2006) as well as in a nonavian vertebrate taxon, the lizard genus Egernia (Duffield and Bull 1996; Manning 2002; Chapple 2005; While et al. 2007—termed birthing asynchrony as Egernia are viviparous, see also Radder and Shine 2007 for discussion of sex-based hatching asynchrony in Bassiana duperreyi). Thus, new systems are emerging in which to examine the selective pressures and evolution of the hatching/birthing asynchrony processes. Specifically, these systems allow us to decouple hypotheses related to adaptive hatching patterns from those that focus on the onset of parental incubation (Smiseth et al. 2006; While et al. 2007).
The above studies have shown that hatching/birthing asynchrony in these nonavian species is not a result of selection on asynchronous incubation (Smiseth et al. 2006), or in the case of Egernia, as a result of embryos developing asynchronously (While et al. 2007). Hatching asynchrony in the burying beetle may still be physiologically constrained because hatching spread is positively correlated with laying spread (Smiseth et al. 2006) and the mechanisms underlying laying spread in the burying beetle are still not fully understood (Smiseth PT, personal communication). However, within Egernia, asynchrony of birthing appears entirely removed from physiological constraints on the asynchronous production of follicles, ovulation, and subsequent embryo development, as asynchrony is first observed at birth (While et al. 2007). Furthermore, when birth of all offspring is induced at the birth of the first offspring, all are born fully developed with no difference in size between offspring (While et al. 2007). Therefore, unlike birds, female Egernia appear to have considerable control over the extent to which they give birth asynchronously.
These observations lead to the suggestions that the occurrence of birthing asynchrony in Egernia has real biological relevance, as birthing asynchrony is not simply a result of constraints on synchronous development (While et al. 2007). This is in line with adaptive explanations of hatching asynchrony in birds, in that it confers a fitness advantage to parents or offspring (see earlier references). An adaptive explanation for birthing asynchrony fits well with our understanding of Egernia behavior. Egernia display relatively complex sociality for reptiles with, considerable variation in social organization both between and within species and even between populations of the same species (e.g., Gardner et al. 2001; Duffield and Bull 1996; O'Connor and Shine 2003; Chapple and Keogh 2006). These social systems are characterized by a highly saturated habitat, leading to intense competition over resources, high levels of aggression between conspecifics, and ultimately high juvenile mortality (Chapple 2003). Although the low level of parental care in Egernia, relative to birds, makes it unlikely that birthing asynchrony evolved as a mechanism to increase parental fitness by decreasing the parental care load (but see O'Connor and Shine 2004), such an intensely competitive and aggressive social environment may select for mechanisms to maximize offspring competitive ability and fitness through increased survival or growth. Birthing asynchrony may act as such a mechanism.
Here we use Egernia whitii to examine whether there are fitness advantages to offspring being born asynchronously versus synchronously. We used the hormone arginine vasotocin (AVT) to induce birth of offspring (Cree and Guillette 1991), thereby allowing us to create both asynchronous and synchronous litters and test for differences in offspring survival and growth between them. Based on hatching asynchrony patterns in birds, we predict that birthing asynchrony will create a size hierarchy within the litter and that this will have flow on effects to offspring survival and size. Specifically, we predict that differences within asynchronous litters will be driven by order of birth, with offspring born earlier gaining significant growth benefits over latter-born offspring, in line with strong hatching order effects in some avian systems (e.g., Badyaev et al. 2002; Johnson et al. 2003; Stienen and Brenninkmeijer 2006).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Study species
The genus Egernia comprises 30 species of skink occurring in a diverse range of habitats throughout Australia and is characterized by relatively large adult and offspring body sizes and delayed maturity (Chapple 2003
). We used the White's skink (E. whitii) from a population on the East Coast of Tasmania, Australia (42°57'S, 147°88'E). Egernia whitii is a medium-sized (75 mm in snout-vent length [SVL]) viviparous species, which occurs in a variety of habitats throughout southeastern Australia. Recent research has shown that the social organization of Tasmanian populations of E. whitii is based around small family groups comprised of a monogamous male/female pair bond (While G, unpublished data) similar to that found in mainland populations (Chapple and Keogh 2006). Parental care in this species extends to semi-independent juveniles remaining within the parental home range postbirth gaining access to resources and potentially protection from infanticide (While G, unpublished data, see also O'Connor and Shine 2004). We have previously documented birthing asynchrony in this species, documenting its occurrence in 100% of litters across 2 reproductive seasons. Females give birth to offspring with an average of approximately 2 days between births; however, spread of births varies both between litters and between years (While et al. 2007). This spread in births is not due to asynchronous development of eggs or embryos and arises from a delay in the parturition of fully developed offspring (While et al. 2007).
Field and laboratory procedures
Sixty female Egernia were captured using mealworm fishing or noosing techniques, at the end of gestation when offspring development was largely complete (late January to early February 2005). Egernia whitii litter sizes range from 1 to 5 throughout their range (Chapple 2003), and from 1 to 4 in Tasmanian populations (While et al. 2007); given our aim was to examine the effects of birthing asynchrony on offspring fitness, we palpated females in the field and retained only those that were judged to carry more than 1 follicle/developing embryo (see While et al. 2007 for details on the frequency of litter sizes within a natural population of E. whitii). Females were returned to the specifically designed terrestrial ecology facilities at the University of Tasmania where they were housed individually in plastic terraria (30 x 60 x 40 cm) in a room maintained at an ambient temperature of 17 °C. Each terrarium was supplied with a basking light on a 10/14 h light and dark cycle, which provided a thermal gradient allowing each female to thermoregulate to their preferred body temperature (
30 °C). Food (Tenebrio larvae, crushed fruit) and water was supplied ad libitum. Females gave birth approximately 2 weeks after being brought into the laboratory.
Prior to the birth of offspring, females were divided into 1 of 3 treatment groups:
- (i) Naturally asynchronous (control),
- (ii) Experimentally asynchronous,
- (iii) Experimentally synchronous.
- (ii) Experimentally asynchronous,
In the naturally asynchronous (i) treatment, females gave birth naturally and therefore asynchronously. In both experimental groups (ii and iii), we followed the same initial protocol. Females gave birth to the first offspring within a litter naturally (cages were checked every hour for birth of offspring during each day). After the birth of the first offspring, it was removed from its mother and housed in an individual terrarium. Females were then given an intraperitoneal injection with the birth hormone AVT to induce birth of remaining offspring (Cree and Guillette 1991). AVT was administered at a dose of 1 µg/g body weight dissolved in 100 µl of lizard ringer solution based on modified protocols from Atkins et al. (2006). After the AVT injection, females were monitored each 30 min for subsequent births; if no births resulted within 2 h of administration, a second dose of AVT was administered (32 required a single dose of AVT and 4 required a second dose of AVT). On the birth of subsequent offspring, they too were removed as per the first-born offspring and housed in individual terrarium. In the experimentally asynchronous (ii) treatment, offspring were introduced back into their mother's terrarium asynchronously. Introduction of the first offspring occurred 2 h after completion of parturition, with subsequent offspring introduced at 2-day intervals (based on the average spread of births in the natural population; While et al. 2007). The order of offspring introduction was randomized with respect to birth order, resulting in each offspring within this treatment having both an introduction and a natural birth order. In the experimentally synchronous (iii) treatment, all offspring were introduced to their mothers' terrarium synchronously, 2 h after the completion of parturition, mimicking birth occurring within hours as in most other skink species (Norris 1997). In all treatments, once back in their mothers' terrarium, both females and offspring remained there for the duration of the experiment. Food was available to offspring at all times; however, as offspring feeding does not usually commence until 2 days after birth (While G, unpublished data), slight differences in feeding regimes between introduced and isolated siblings should not confound results on growth or survival.
At birth, offspring weight (±1 mg), SVL, and total length (±1 mm) were recorded. For offspring in all treatments, order of birth was recorded, and for offspring in the naturally asynchronous treatment, spread of birth within a litter was also recorded. Although it is now recognized that squamates are relatively easy to sex at birth (Harlow 1996; Wapstra et al. 2004), this is not the case for Egernia species, as both sexes appear to retain well-developed hemipenes until well after birth (Chapple 2005), and thus we could not record offspring sex, precluding further tests of sex-specific hypotheses (e.g., Badyaev et al. 2002; Johnson et al. 2003; Lezalova et al. 2005). After birth, all females and their offspring were housed in their terrarium for a 6-week period. Food and water was available ad libitum so that neither of these resources were limiting. Growth rate and survival of offspring was assessed over this period. Six weeks was chosen because it allowed for an appropriate length of time for treatment effects to become apparent (e.g., Wapstra 2000; Olsson and Shine 2002). At the 6-week period, data had been collected on mortality, size (mass, SVL, litter average, and largest in litter), and growth rate (mass and SVL). As growth in squamates is typically linear early in life (Andrews 1982; Wapstra 2000), growth rate of offspring was calculated simply as the slope of the offspring mass versus time plot. Mean mass at 6 weeks was highly correlated with mass growth rate, as well as SVL, (Pearsons correlation coefficient, all P < 0.0001, r > 0.70), thus for larger models we report only results for mass at 6 weeks. As asynchronous hatching in birds normally results in the establishment of a size hierarchy within the clutch (Stenning 1996), we calculated a litter mass hierarchy as ([mass of the largest in the litter – mass of the smallest in the litter]/average mass of the litter x 100) (e.g., Vinuela 1996), at birth and 3 weeks (only for litters that had all offspring surviving). Thus, we have an estimate of the mass hierarchy within the litter and an individual's position within a hierarchy (1st or last) both at birth and at 3 weeks. The terrarium was checked twice daily for offspring mortality, and offspring were re-measured every 5 days. At 6 weeks after completion of the experiment, females and their offspring were returned to their exact site of capture.
Statistical analysis
Differences between treatments
Differences in survival between treatments were analyzed using generalized linear mixed models (GLMMs) using PROC GLIMMIX in SASSTAT v.9.2 using a binomial distribution and a logit link function (Littell et al. 1996). We included the survival state of the offspring at 6 weeks as the dependent variable, female identity nested within treatment as the random factor, treatment as a fixed factor, and mass at birth as a covariate. Significance of fixed effects was tested using F-tests, with the degrees of freedom calculated using the Satterthwaite's approximation (Littell et al. 1996). Differences in the rate of survival between treatments were further examined using a cox-proportional hazards model using the PHREG procedure in SASSTAT.
As differences in survival between treatments may also cause differences in offspring size, if the death of a sibling increases growth rate of the surviving sibling (e.g., through greater access to resources), sibling death, and the time since death may need to be controlled for in any analysis of size differences. To establish whether this was the case, we examined growth rates of offspring before and after sibling death. We found no difference in growth rate of surviving offspring before and after sibling death (slope of growth rate pre–sibling death 0.004 ± 0.002 mg/day, slope of growth rate post–sibling death 0.007 ± 0.002, paired t-test, t = –1.3208, P = 0.11, n = 10), therefore allowing us to continue the analysis of offspring size without controlling for sibling death or time since sibling death.
Offspring size was analyzed at both an individual (mass at 6 weeks) and litter level (mass of largest individual within a litter). Differences in offspring size between treatments at an individual level were analyzed using GLMMs using the PROC MIXED procedure in SAS, with offspring mass at 6 weeks as the dependent variable, female identity nested within treatment as the random factor, treatment as a fixed factor, and mass at birth as a covariate. Differences between treatments in the mass of the largest offspring in a litter was carried out using a general linear model using PROC GLM in SAS with the mass of the largest offspring as the dependent variable and treatment as a fixed factor.
Differences within treatments
For within-treatment differences in offspring size, growth, and survival, we included 2 factors as predictors; individual position within the litter mass hierarchy and birth order, as well as appropriate covariates. Position within the litter mass hierarchy calculated at 3 weeks, instead of birth, was used because it allowed adequate time for both the hierarchy itself to become established and the position of each sibling within that hierarchy to be determined. Although birth hierarchy was maintained in some of these cases, it was not in all (spearman's rank correlation, r2 = 0.23), suggesting other factors may play a role in determining an individual's position in the hierarchy. Therefore, as we do not yet understand how the hierarchy is established and how an individual's position within the hierarchy is determined (see also Results), we used hierarchy characteristics at 3 weeks when hierarchies were established. An accurate estimate of an individual's position within the litter mass hierarchy is important as it has significant flow on effects to within-litter behavioral interactions, resulting in spatial segregation between siblings, with smaller individuals suffering decreased basking opportunities, decreased feeding rates, and increased antagonistic behavior from larger siblings (While G, unpublished data). Birth order was included as a predictor for the 2 asynchronous treatments (natural and experimental) and hereafter refers to the natural order of birth in naturally asynchronous treatments and order of introduction in experimentally asynchronous treatments. As both experimental treatments (asynchronous and synchronous) also have a natural birth order (first-born offspring were born naturally), which may be important in predicting offspring survival and size, we reran all models with natural birth order as a predictor for all treatments. Natural birth order was not found to be a significant predictor of size or survival in any of the treatments.
Differences in survival and offspring size within treatments were analyzed using GLMMs using PROC GLIMMIX and GLMMs using PROC MIXED in SASSTAT v.9.2, respectively, the former using a binomial distribution and a logit link function (Littell et al. 1996). We included the survival state and mass of the offspring at 6 weeks as the dependent variables, female identity as the random factor, birth order, and position within the litter mass hierarchy at 3 weeks as fixed factors, and mass at birth as a covariate. For analysis of survival within the synchronous treatment, we entered only position within the litter mass hierarchy at 3 weeks as a fixed factor as all offspring were born together in this treatment. For analysis of survival state, we pooled the experimentally asynchronous and naturally asynchronous treatments as examination of the least squares means differences in the between-treatment survival analysis showed that they did not differ from one another. Significance of fixed effects was tested using F tests, with the degrees of freedom calculated using the Satterthwaite's approximation (Littell et al. 1996).
All models started with the full model including all interactions terms and we subsequently eliminated factors backward, starting with higher order interaction terms, at P values > 0.25 (Quinn and Keogh 2002). We report here the results for full models containing all main effects, after removal of nonsignificant interaction terms. All data were checked for violations of assumptions, including homogeneity of slopes for mass at birth, and no data required transformation. Means and standard errors (SEs) are reported throughout. Due to mortality of offspring throughout the experiment, sample sizes differed between analyses.
Ethical considerations
All research carried out was done so with approval of the Animal Ethics Committee of the University of Tasmania (Protocol No. A0008524) and under Tasmanian national parks permits (Permit No. FA 06538).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Of the 60 females brought into the laboratory to give birth, 52 did so resulting in 114 offspring distributed among the 3 treatments. This comprised of 16 females in the naturally asynchronous treatment giving birth to 35 offspring (average litter size 2.18 ± 0.10), 18 females in the experimentally asynchronous treatment giving birth to 38 offspring (average litter size 2.11 ± 0.07), and 18 females in the experimentally synchronous treatment giving birth to 41 offspring (average litter size 2.27 ± 0.10). The remaining 8 females either failed to give birth (n = 5), gave birth to only 1 offspring (n = 2), or gave birth to stillborn young (n = 1). Average spread between births was fixed in both the experimentally synchronous (0 days) and the experimentally asynchronous (2 days) treatments, but ranged from 1 to 5 days in the naturally asynchronous treatment (mean 1.75 ± 0.29). There was no difference in offspring mass at birth between treatments (F2,49 = 1.65, P = 0.20, Table 1), or within the treatments, between birth order position (F2,109 = 0.28, P = 0.76). There was also no difference at birth, between treatments, in the largest offspring within a litter (F2,51 = 1.01, P = 0.37, Table 1). Litter mass hierarchy did not differ significantly between treatments at birth (F2,51 = 0.05, P = 0.95, Figure 1); however, at 3 weeks, as predicted by avian studies, experimental introduction of offspring synchronously resulted in less of a hierarchy than offspring introduced with a normal spread in births (experimentally asynchronous vs. experimentally synchronous treatment, F1,27 = 4.83, P = 0.03, Figure 1).
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Survival and size differences between treatments
At 6 weeks, 71 of the 114 offspring (62%) had survived. There was a significant effect of treatment on offspring survival (F2,53.08 = 5.28, P = 0.008), with offspring from asynchronous treatments (natural and experimental) experiencing significantly greater mortality (40% and 53%, respectively) than those in the synchronous treatment (22%) based on least squares means differences (Figure 2). These results were mirrored in our cox-proportional hazards model analysis, which showed a significant difference in survival rates (P = 0.01) between asynchronous (natural and experimental combined) and synchronous treatments in the rate of mortality, with the hazards ratio indicating that the rate of mortality in asynchronous treatments was significantly greater than that of synchronous treatments (hazards ratio: 0.39).
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Offspring mass at 6 weeks also differed significantly between treatments (F2,67 = 8.61, P = 0.0005, Table 1), with offspring from experimentally asynchronous treatments being heavier than those in either the naturally asynchronous or the experimentally synchronous treatments based on examining the least squares means differences (Figure 3). Offspring in the naturally asynchronous treatments had a greater mass on average than those in the experimentally synchronous treatments, but this difference was not significant. Growth rates of offspring over the 6 weeks were also significantly different between treatments (F2,67 = 8.63, P = 0.0004, Table 1), with offspring in experimentally asynchronous treatments showing a 17% increase in body mass over the 6 weeks compared with 3% and 6% in the naturally asynchronous and experimentally synchronous treatments, respectively. The same pattern emerged for the largest offspring in a litter, with the largest offspring from the experimentally asynchronous litters being significantly larger than those in either the naturally asynchronous or the experimentally synchronous treatments (F2,43 = 5.50, P = 0.01, Table 1, Figure 3).
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Survival and size differences within treatments
We then examined what may be promoting the differences between treatments in offspring size and survival by examining more closely within-treatment effects. Based on avian hatching asynchrony literature, the most likely explanation for the differences in size and survival between treatments was a birth order effect in the asynchronous litters. However, within these litters, there was no effect of birth order (1st, 2nd, or 3rd) on either survival (F2,41 = 0.77, P = 0.47) or offspring mass at 6 weeks (experimentally asynchronous: F1,9 = 0.08, P = 0.79; naturally asynchronous: F2,12 = 0.81, P = 0.47).
Offspring survival at 6 weeks was predicted by position within the litter mass hierarchy at 3 weeks in the asynchronous treatments (F1,41 = 5.83, P = 0.02, Table 2), with the smallest offspring in the hierarchy suffering the greatest mortality (55% mortality of the smaller offspring vs. 21% mortality of the larger offspring). Neither position within the litter mass hierarchy (F1,20.7 = 2.26, P = 0.15, Table 2) nor mass at birth (F1,20.7 = 0.18, P = 0.67, Table 2) predicted offspring survival in synchronous litters.
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Offspring mass at 6 weeks was determined by mass at birth for both the naturally and the experimentally asynchronous treatments (naturally asynchronous: F1,12 = 5.71, P = 0.03, r2 = 0.28; experimentally asynchronous: F1,9 = 6.81, P = 0.03, r2 = 0.17, Table 3), with mass at 6 weeks increasing as a function of mass at birth (Figure 4). Position in the litter mass hierarchy at 3 weeks was marginally significant in explaining mass at 6 weeks in the naturally asynchronous treatment (F1,12 = 4.44, P = 0.06, Table 3) but not in the experimentally asynchronous treatment (F1,9 = 1.23, P = 0.29). The lack of a position within the hierarchy effect on offspring mass at 6 weeks in the experimentally asynchronous treatment may be based on the low sample size of the smallest offspring (due to increased mortality: n = 3). Both position within the mass hierarchy (F1,23 = 4.30, P = 0.06, Table 3) and mass at birth (F1,23 = 3.99, P = 0.06, Table 3) were also marginally significant in predicting 6-week offspring mass in synchronous treatments. Position within the litter mass hierarchy was not predicted by mass at birth (F1,78 = 2.44, P = 0.12) or correlated with birth order in asynchronous treatments (Spearman's rank correlation, P = 0.87).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Recent research has identified a number of nonavian taxa in which hatching asynchrony, or processes analogous to hatching asynchrony (i.e., birthing asynchrony), occur (Nalepa 1988
; Muller and Eggert 1990; Smiseth et al. 2006; While et al. 2007). To date, this research has remained descriptive solely documenting the extent of asynchronous hatching/birthing in the respective taxa. Here we provide the first experimental test of the potential advantages to offspring of hatching/birthing asynchrony in a nonavian system in an attempt to provide explanations for its evolution.
Our results showed that offspring in asynchronous treatments (both naturally asynchronous and experimentally asynchronous) suffered increased mortality compared with those offspring introduced synchronously, with almost 50% greater mortality in experimentally asynchronous litters compared with experimentally synchronous litters. Mortality within litters appeared to be a function of aggression between conspecifics resulting in decreased basking and feeding rates, loss of condition, and eventually starvation of 1 sibling (While G, personal observation). Similar causes of mortality have been found in asynchronously hatching bird species, usually resulting from intense competition for food provided by parents (e.g., Mock and Parker 1998; Vinuela 2000). In contrast to mortality results, surviving offspring in experimentally asynchronous litters benefited from increased growth to 6 weeks compared with those in the experimentally synchronous treatment. These differences in size were independent of differences in mortality between treatments, which could potentially reduce estimates of average offspring mass because of the significant differences observed between treatments in the largest individual within a litter, suggesting that there were also significant differences between treatments in the "best" offspring. These results suggest that the observed differences between treatments in size are real.
Although the above results held for offspring in the experimentally asynchronous treatments, the same pattern was not observed for the naturally asynchronous treatments, where offspring appear to suffer both increased mortality and decreased growth rate when compared with the 2 experimental treatments. One potential explanation for the discrepancies between the results in naturally and experimentally asynchronous treatments is that similar patterns were occurring in both treatments, decreased survival but increased size of the largest offspring, but at a slower rate in the naturally asynchronous treatment. That is, the lower mortality rate at 6 weeks in naturally asynchronous treatment versus the experimentally asynchronous treatment could have affected our estimation of growth rate due to the survival of the smaller offspring. However, the largest offspring in the litter (which is independent of mortality rates) also differed between the 2 asynchronous treatments, suggesting that this may not be the only explanation. Alternatively, differences could be a result of an interruption, due to the experimental protocol, of the mother–offspring bond formed after birth, which has been shown to be an important determinant of growth, development, and dispersal in social lizards (e.g., Lena et al. 1998; Le Galliard et al. 2003; Cote et al. 2007). If these interactions were driving the differences in growth and development between treatments then we would expect that the strongest differences in growth and survival to be between the natural and experimental treatments, but this was not the case. Differences could also be a function of the variation in birth spread in naturally asynchronous litters (range 1–5) compared with experimentally asynchronous treatments (where spread was fixed at 2 days), which itself could have had differing effects on offspring size and survival. Spread between offspring has been shown to be a strong determinant of the strength of conspecific competition in birds, with larger spread leading to increased size hierarchies, and flow on effects to offspring fitness (e.g., Mock and Ploger 1987; Hillstrom et al. 2000; Vinuela 2000). Although we do not know the extent to which the length of time between births affects offspring fitness in Egernia, it is possible that this may account for some of the variation between the naturally and the experimentally asynchronous treatments.
The above between-treatment differences in mortality and mass were driven primarily by offspring size differences created by the development of a greater mass hierarchy within asynchronous compared with synchronous litters and offspring mass at birth. This resulted in the relatively smaller offspring in asynchronous treatments suffering both an increased risk of mortality and decreased mass at 6 weeks. The establishment of a size hierarchy within a litter/clutch and its associated effects on survival lends itself to brood reduction arguments commonly developed for avian species. These suggest that hatching asynchrony serves as a mechanism to allow for simple brood reduction in years of limiting resources (Lack 1954; Magrath 1989). However, although some authors argue the loss of an individual from a clutch provides relief to the remaining offspring in terms of increased resources resulting in an increased opportunity for growth (Hillstrom and Olsson 1994; Stoleson and Beissinger 1997), our results showed that the growth rate of offspring throughout the 6 weeks was independent of sibling death, that is, growth rate did not increase after the death of a sibling. This supports more recent research, which suggests that hatching asynchrony creates 2-track offspring: core offspring, which do well irrespective of what their siblings do, and marginal offspring, whose survival and growth are reliant on resource levels (Forbes and Glassey 2000). Although position within the litter mass hierarchy at 3 weeks and mass at birth were important for explaining mortality and mass at 6 weeks in asynchronous litters (natural and experimental), this was not the case in synchronous litters. In synchronous litters, the absence of clear size hierarchies may lead to continued competition between siblings, the energy expenses of this competition potentially explaining the slower growth in these litters (Vinuela 2000). However, both position within the litter mass hierarchy and mass at birth were only marginally nonsignificant in predicting mass at 6 weeks in the synchronous litters and therefore may still be important determinants of offspring mass, although not to the same extent, or over the same time scale, as in asynchronous litters.
One aspect of the above patterns, which remains unresolved, is the mechanism by which they are produced. In avian systems, order of hatching is the mechanism that governs offspring size and survival with the first-hatched chick gaining the advantage over later-hatched chicks through early growth, resulting in strong hatching order effects on both survival and growth rate (e.g., Badyaev et al. 2002; Johnson et al. 2003; Stienen and Brenninkmeijer 2006). Surprisingly, within asynchronous litters, we found no link between birth order and mortality, mass at 6 weeks, or any factors that affected either of these, such as the position within the litter mass hierarchy at 3 weeks. Although Vinuela (2000) argues that hierarchies may still develop independent of birth order effects, through differential growth, with the establishment of size hierarchies potentially dependent on early fights between siblings, or slight differences in physical condition or behavior (Amundsen and Slagsvold 1991; Laaksonen 2004), it is difficult to understand how this would occur in asynchronous litters but not in synchronous litters. This suggests that, although giving birth asynchronously does not change the competitive ability of offspring per se, it does change the level of competition within the litter. This increased competitive environment leads to an increased importance of offspring mass at birth and the establishment of a litter size hierarchy in predicting both offspring growth and survival. From a parent–offspring conflict perspective, the absence of a birth order effect in a viviparous species is understandable. If the asynchrony has a predictable outcome, that is, first-born offspring always win, generating strong negative effects of being born second, then we would expect strong selection on a mechanism to avoid being born later (e.g., offspring control over the timing of parturition). Unlike bird embryos, which have no contact with each other and no control over the timing of hatching due to the constraints of egg development, such a mechanism could presumably evolve in viviparous species. Although we do not yet know to what extent embryos control the timing of birth, recent evidence from mammals suggests that they may play an important role (Johnson and Everitt 1988; Shaw and Renfree 2001), and there is the potential for similar mechanisms to occur in squamates (Girling and Jones 2006).
What do these results tell us about the potential adaptive function of birthing asynchrony in E. whitii? They suggest that the occurrence (and possibly the degree) of birthing asynchrony represents a trade-off between its costs and benefits. Synchronous litters were more successful than asynchronous litters in terms of survival, with almost twice as many offspring surviving to 6 weeks, but they had reduced mass at 6 weeks (when compared with experimentally asynchronous litters). Whether the reproductive cost incurred by decreased offspring survival is compensated by the increase in mass in the long term is currently unknown. A similar pattern to the above has also been observed in a number of avian systems where, in terms of offspring survival, synchronous litters fledge as many, or more, offspring than asynchronous litters (Stoleson and Beissinger 1997; Wiehn et al. 2000). However, although analogous results in avian taxa are often explained in terms of brood reduction being advantageous only in times of food limitation (Pijanowski 1992), our results may be relatively easier to explain. Although our experimental protocol dictated that offspring were confined to their mothers' terrarium postbirth, in natural situations smaller offspring may have the opportunity to disperse from their natal home range as soon as they are born, as occurs in the majority of reptile taxa (e.g., Olsson and Shine 2003; Ryberg et al. 2004). Therefore, in a natural setting, the cost of being relatively small is unlikely to be decreased chance of survival, but dispersal out of the natal home range and away from potential protection from infanticide and access to thermal and nutritional resources (e.g., Bull and Baghurst 1998; O'Connor and Shine 2004). If this is the case, then birthing asynchrony may serve as a mechanism to increase phenotypic variation within a litter, producing offspring that will follow variable life history or dispersal strategies, which may be advantageous in spatially or temporally unpredictable environments (e.g., Laaksonen 2004). Testing these hypotheses in the field represents one of the key next steps in understanding the evolution of birthing asynchrony in this taxon.
Our results do, however, provide a starting point for addressing the evolution of birthing asynchrony in Egernia. We believe the links to Egernia's relatively complex sociality are hard to ignore, as both of these features are uncommon in reptiles (While et al. 2007). Egernia social systems are characterized by a highly saturated habitat, leading to intense competition over resources, high levels of aggression between conspecifics, and ultimately high juvenile mortality (Chapple 2003). Such a social environment provides strong election for mechanisms to maximize offspring fitness through increased survival or growth. If early growth rate is linked to either survival, age at maturity, or indirect measures of fitness (e.g., home range acquisition or size), as it is in other squamate species (e.g., Sinervo and Doughty 1996; Olsson and Shine 1997; Olsson and Madsen 2001), then it may pay females to favor 1 offspring by allowing it to remain in the natal home range. This is consistent with research in other Egernia species, for example, Egernia stokesii, which has shown that the benefits of group living are not shared equally among all social group members, with subordinate members exhibiting decreased basking and activity times (Lanham 2001). Why only 1 offspring appears to benefit from this behavior is yet to be investigated. However, birthing asynchrony and brood reduction may represent the parental rather than offspring optima (Horak 1995; Hebert and McNeil 1999). Whether this is the case in Egernia is unknown and probably unlikely given the relatively low level of parental care exhibited in most squamates (Huang 2007). However, the level of parental care in Egernia is higher than in many other reptile species and extends to semi-independent offspring remaining close to 1 or both parents gaining access to resources and potentially protection from infanticide (Bull and Baghurst 1998; O'Connor and Shine 2004). Furthermore, recent research has shown that some reptile females actively defend offspring from conspecifics and predation through increased aggression during egg laying (Huang 2007) or at parturition (Greene et al. 2002; While G et al., unpublished data). Therefore, from a parental care perspective, permitting more than 1 offspring to stay may actually incur a significant energetic cost and potentially an increase in predation risk, which itself may have carry-over effects to future reproductive events.
Birthing asynchrony in this species appears to be a trade-off between the costs, in terms of offspring mortality/dispersal, and the benefits, in terms of offspring mass and growth, both of which result from the size hierarchy produced by asynchronous birth as well as offspring mass at birth. Although we are yet to determine the mechanism by which these birthing asynchrony patterns are produced, demonstrating the cost and benefits of asynchronous versus synchronous birthing allows us to begin to speculate as to the potential adaptive function of birthing asynchrony in E. whitii and provide a starting point for addressing its evolution within this and other Egernia species. Certainly, the strong concordance between sociality within Egernia and the presence of birthing asynchrony is hard to ignore—both of these features are uncommon in reptiles. Future work should expand on this starting point and examine the potential social and environmental factors, which affect birthing asynchrony behavior in this taxon, while continuing to examine the behavioral and physiological mechanisms, which may promote it. In doing so, we may also gain insights into the evolution and maintenance of hatching asynchrony in other systems.
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Holsworth Wildlife Research Fund (W0014499), Joyce Vickery Research Fund, and Environmental Futures Network (RN0457921), all allocated to G.M.W.
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ACKNOWLEDGEMENTS |
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We thank David Sinn and Tobias Uller for discussion of ideas, statistical advice, and detailed comments on earlier versions of the Manuscript, Sue Jones for assistance with physiological components of the experimental design; and Jemina Stuart-Smith, Amelia Hall, Nigel Upston, and Stephen While for help collecting lizards in the field. We also thank 3 anonymous reviewers for comments on earlier versions of the Manuscript. This research was carried out with approval of the Animal Ethics Committee of the University of Tasmania (Protocol No. A0008524), under Tasmanian national parks permits (Permit No. FA 06538).
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