THE EVOLUTION OF REPRODUCTIVE EFFORT IN LIZARDS AND SNAKES

Life history theory suggests that the optimal evolved level of reproductive effort (RE) for an organism depends upon the degree to which additional current reproductive investment reduces future reproductive output. Future reproduction can be decreased in two ways, through (i) decreases in the organism's survival rate, and/or (ii) decreases in the organism's growth (and hence subsequent fecundity). The latter tradeoff–that is, the “potential fecundity cost”—should affect the evolution of RE only in species with relatively high survival rate, a relatively high rate of fecundity increase with body size, or a relatively high reproductive frequency per annum. Unless these conditions are met, the probable benefit in future fecundity obtained from decreasing present reproductive output is too low for natural selection to favor any reduction in RE below the maximum physiologically possible. Published data on survival rate, reproductive frequency and relative clutch mass (RCM) suggest that many lizard species fall well below the level at which natural selection can be expected to influence RE through such “potential fecundity” tradeoffs. Hence, the relative allocation of resources between growth and reproduction is unlikely to be directly optimized by natural selection in these animals. Instead, energy allocation should influence the evolution of RE only indirectly, via effects on an organism's probability of survival during reproduction. Survival costs of reproduction may be the most important evolutionary determinants of RE in many reptiles, and information on the nature and extent of such costs is needed before valid measures of reptilian RE can be constructed.     

Potential ‘costs of reproduction’ in a skink: Inter‐ and intrapopulational variation

Reproductive costs are important determinants of reproductive effort in squamate reptiles. Consequently, differences in costs of reproduction between populations of geographically or climatically widespread species are likely to result in different patterns of reproductive effort. In the present study, the effect of pregnancy on sprint speed was examined in a small viviparous skink, Niveoscincus ocellatus (Gray 1845), from two populations at the climatic extremes of its distribution. Decreased sprint speed has the potential to be an important cost of reproduction in this species, through a reduced ability to avoid predation and/or decreased foraging efficiency. Lizards inhabiting the colder site were larger than those from the warmer site and, contrary to predictions from life history theory, had a higher reproductive effort. In both populations, sprint speed was lower in pregnant lizards than in either the same individuals after birth or non‐pregnant control lizards. Within each population, sprint speed was unrelated to the level of reproductive effort of the female in terms of either absolute mass of the reproductive burden or the burden relative to her post‐partum body mass. However, within each population, the mass of the clutch that an individual female was carrying relative to snout–vent length was an important determinant of her sprint speed while pregnant. Thus, within each population, a relatively high reproductive burden may potentially increase costs of reproduction in this species. Despite this relationship and predictions from life history theory suggesting that annual reproductive effort will be lower in populations with a large body size and delayed maturity, it is suggested that a higher reproductive effort at the cold site is possible because they have a higher absolute sprint speed because of their larger size and a relatively higher abundance of cover at the cold site, and differences in predation pressure may alter selective pressures on reproductive investment.     

Reproductive strategies and body shape in the European pond turtle (Emys orbicularis) from contrasting habitats in Italy

Comparisons within and among populations offer important insights into variation in life-history traits and possible adaptive patterns to environmental conditions. We present the results of observed differences in body size, body shape and patterns of reproduction in four separate populations of the European pond turtle Emys orbicularis in central and southern Italy – coastal ( n =3) and mountainous ( n =1) sites and pond ( n =2) and canal ( n= 2) habitats – to determine whether phenotypic plasticity affects reproductive output. Although we did not find any significant latitudinal variation in body size, we observed significant differences in body shape between canal (rounded body shape) and pond (elongated body shape) systems and smaller size with rounded shape in the mountainous population. Reproductive output is similar among populations (median=5 eggs per clutch), whereas reproductive investment (relative clutch mass to maternal body mass) is higher in the mountain population (one clutch per year) than in coastal populations (two clutches per year), suggesting differential trade-offs between geographic locality, elevation and habitat type. Turtle shell shape and geographic location together affect reproductive output in E. orbicularis in Italy.     

Effects of pregnancy on locomotor performance: an experimental study on lizards

Pregnancy is associated with reduced locomotor performance in many types of animals, but we do not know to what degree this correlation is caused by simple physical burdening, versus physiological changes associated with pregnancy, or to confounding variables (such as season or female body size) that simultaneously influence both reproductive investment and locomotor speeds. To identify causal effects of burden on locomotion, we need to experimentally manipulate the size of the load being carried. Injection of sterile fluid into the peritoneal cavities of 84 garden skinks (Lampropholis guichenoti) showed that speeds decreased with increasing burdens. Lizards with a burden equivalent to 25% of their body mass ran about 15% slower, mirroring the situation seen in gravid lizards of this population. Thus, simple physical burdening appears to be the primary causal component of the locomotor cost of reproduction within these animals. A lizard's sex, body size and shape had little effect on its running ability either before or after treatment, but faster lizards showed a greater performance decrement after burdening than did their slower conspecifics.     

Locomotor impairment of gravid lizards: is the burden physical or physiological?

Pregnancy is associated with reduced locomotor performance in several reptile species, but the reasons for this reduction remain unclear. Previous authors generally have assumed that the decreased maternal mobility is due to the physical burden of the clutch, but our data on a viviparous Tasmanian scincid lizard (Niveoscincus microlepidotum) suggest a different interpretation. Running speeds of gravid female skinks decrease during gestation (as litter mass increases), but this locomotor impairment is due to physiological changes associated with pregnancy, rather than simple physical burdening. Maternal running speeds are unrelated to litter masses, and do not increase in the week after parturition. Females with very large abdominal fat‐bodies (due to ad libitum feeding in the laboratory), equivalent in mass to the litter, nonetheless run rapidly. If the locomotor ‘costs’ of reproduction reflect all‐or‐none physiological changes associated with pregnancy, then the magnitude of such costs may correlate only weakly with the actual level of reproductive investment. Because life‐history models predict that the relationship between fecundity and ‘cost’ has important evolutionary consequences, our results highlight the need to clarify the causal basis for locomotor impairment in gravid reptiles.     

Association between haematozoan infections and reproduction in the Pied Flycatcher

1. Parasites may affect breeding success of their host since they compete for the same resources as their hosts. Reproduction may also increase the susceptibility of a host to parasite infections owing to lowered resistance to parasites during breeding.
2. We studied the association between breeding performance and haematozoan parasite infection in the Pied Flycatcher ( Ficedula hypoleuca ) by using both natural data on reproduction and data from clutch size manipulations.
3. The most frequent blood parasites of the Pied Flycatcher in central Finland were Haemoproteus pallidus , Haemoproteus balmorali and Trypanosoma avium complex.
4. We did not find evidence that these haematozoan parasites have any debilitating effects on either reproduction or survival. The variation in reproductive effort did not seem to influence susceptibility to new blood parasite infections.
5. The intensity of Haemoproteus balmorali tended to increase in infected males as the brood size was artificially enlarged. Also, in females intensity of H. pallidus infection tended to increase with the level of clutch size manipulation. Thus, increased reproductive effort seems to debilitate the ability of Pied Flycatcher to control chronic infections.
6. Individuals with enlarged clutches/broods increased their reproductive effort at the expense of defence towards parasites. The cost of current reproduction may then be at least partly mediated by haematozoan infections.     

Phenotypic plasticity in reproductive traits induced by food availability in a lacertid lizard, Takydromus septentrionalis

Understanding the proximate determinants of phenotypic variations in life-history traits can provide powerful insights into a species' life-history strategies. I experimentally manipulated availability of food (high vs low) to examine plasticity in the reproductive traits of northern grass lizards, Takydromus septentrionalis (Lacertidae), from eastern China. Food availability significantly affected reproductive frequency and thereby seasonal reproductive output, but had little effect on reproductive output per clutch. Low-food females postponed reproduction and produced less clutches in the reproductive season than did high-food females. After producing their second clutches, low-food females were in lower body condition than the high-food counterparts. By the end of the experiment, however, all females exhibited similar body condition. Clutch size and clutch mass differed between the first and second clutches but not between the treatments. Egg size and phenotypic traits of hatchlings (body size, morphology and locomotor performance) in T. septentrionalis did not vary significantly from first to second clutches nor between the two treatments. These results support optimal egg size (offspring) theory. Female T. septentrionali s "decide" whether or not to reproduce largely based on current energy intake; lowered feeding rates thus delay oviposition and reduce reproductive frequency. In contrast, clutch size, egg size and relative clutch mass remain unchanged.     

Insular shifts and trade-offs in life-history traits in pond frogs in the Zhoushan Archipelago, China

Island and mainland populations of animal species often differ strikingly in life-history traits such as clutch size, egg size, total reproductive effort and body size. However, despite widespread recognition of insular shifts in these life-history traits in birds, mammals and reptiles, there have been no reports of such life-history shifts in amphibians. Furthermore, most studies have focused on one specific life-history trait without explicit consideration of coordinated evolution among these intimately linked life-history traits, and thus the relationships among these traits are poorly studied. Here we provide the first evidence of insular shifts and trade-offs in a coordinated suite of life-history traits for an amphibian species, the pond frog Rana nigromaculata . Life-history data were collected from eight islands in the Zhoushan Archipelago and neighboring mainland China. We found consistent, significant shifts in all life-history traits between mainland and island populations. Island populations had smaller clutch sizes, larger egg sizes, larger female body size and invested less in total reproductive effort than mainland populations. Significant negative relationships were found between egg size and clutch size and between egg size and total reproductive effort among frog populations after controlling for the effects of body size. Therefore, decreased reproductive effort and clutch size, larger egg size and body size in pond frogs on islands were selected through trade-offs as an overall life-history strategy. Our findings contribute to the formation of a broad, repeatable ecological generality for insular shifts in life-history traits across a range of terrestrial vertebrate taxa.     

Costs of reproduction in a tropical invariant-clutch producing lizard (Carlia rubrigularis)

Reproduction involves costs and benefits, whereby increased expenditure into current reproduction can reduce future reproductive success. Costs of reproduction, often assessed using the reduction in locomotor speed, have become well established in temperate-zone lizard species. However, substantial differences in biotic conditions and life-history traits between temperate- and tropical-zone lizards suggest that such costs may be different or of less importance for tropical species. This study examined the effects of reproduction on locomotor speed in the tropical invariant-clutch producing lizard Carlia rubrigularis . Counter to predictions and despite a low relative clutch mass (RCM), gravid and post-oviposition females experienced a reduction in locomotor speed with a physiological basis that was unrelated to the level of reproductive investment. In addition, gravid and postoviposition females exhibited locomotor speeds that were inversely related to the timing of oviposition and approached the speed of non-reproductive females after 3 weeks of oviposition. These results suggest that in addition to RCM, selection may act to reduce the period of recovery in species with extended reproductive seasons and which make numerous bouts of reproduction, such as C. rubrigularis .     

THE EVOLUTION OF REPRODUCTIVE EFFORT IN SQUAMATE REPTILES: COSTS,TRADE-OFFS,AND ASSUMPTIONS RECONSIDERED

We evaluated Shine and Schwarzkopf's (SS) model of the evolution of reproductive effort (RE) in squamate reptiles. They suggested that fecundity trade-offs were unimportant in the evolution of RE in most squamate reptiles and that only survival trade-offs needed to be considered. However, we show that by assuming no variation in offspring size exists, and that adult mortality is episodic, the results of the SS model are not general. By extension, we argue that conclusions drawn about factors important in the evolution of RE in squamate reptiles are premature. Using a modified version of the SS model, we demonstrate that variation in the form of trade-offs relating offspring size and survival substantially affect relationships among clutch size, relative clutch mass, and lifetime reproductive success. We also demonstrate that the way in which adult mortality is simulated drastically affects conclusions about the potential fecundity trade-offs experienced by populations of squamate reptiles. Finally, we suggest that a complete understanding of the evolution of RE will come from theory that incorporates trade-offs between offspring size and quality, as well as other system-specific constraints on the allocation of energy to growth, maintenance, storage, and reproduction.     

Contrasting life histories in neighbouring populations of a large mammal

Background

A fundamental life history question is how individuals should allocate resources to reproduction optimally over time (reproductive allocation). The reproductive restraint hypothesis predicts that reproductive effort (RE; the allocation of resources to current reproduction) should peak at prime-age, whilst the terminal investment hypothesis predicts that individuals should continue to invest more resources in reproduction throughout life, owing to an ever-decreasing residual reproductive value. There is evidence supporting both hypotheses in the scientific literature.

Methodology/Principal Findings

We used an uncommonly large, 38 year dataset on Alpine chamois (Rupicapra rupicapra) shot at various times during the rutting period to test these two hypotheses. We assumed that body mass loss in rutting males was strongly related to RE and, using a process-based approach, modelled how male relative mass loss rates varied with age. For different regions of our study area, we provide evidence consistent with different hypotheses for reproductive allocation. In sites where RE declined in older age, this appears to be strongly linked to declining body condition in old males. In this species, terminal investment may only occur in areas with lower rates of body mass senescence.

Conclusions/Significance

Our results show that patterns of reproductive allocation may be more plastic than previously thought. It appears that there is a continuum from downturns in RE at old age to terminal investment that can be manifest, even across adjacent populations. Our work identifies uncertainty in the relationship between reproductive restraint and a lack of competitive ability in older life (driven by body mass senescence); both could explain a decline in RE in old age and may be hard to disentangle in empirical data. We discuss a number of environmental and anthropogenic factors which could influence reproductive life histories, underlining that life history patterns should not be generalised across different populations.     

Rain,prey and predators: climatically driven shifts in frog abundance modify reproductive allometry in a tropical snake

To predict the impacts of climate change on animal populations, we need long-term data sets on the effects of annual climatic variation on the demographic traits (growth, survival, reproductive output) that determine population viability. One frequent complication is that fecundity also depends upon maternal body size, a trait that often spans a wide range within a single population. During an eight-year field study, we measured annual variation in weather conditions, frog abundance and snake reproduction on a floodplain in the Australian wet-dry tropics. Frog numbers varied considerably from year to year, and were highest in years with hotter wetter conditions during the monsoonal season (“wet season”). Mean maternal body sizes, egg sizes and post-partum maternal body conditions of frog-eating snakes (keelback, Tropidonophis mairii, Colubridae) showed no significant annual variation over this period, but mean clutch sizes were higher in years with higher prey abundance. Larger females were more sensitive to frog abundance in this respect than were smaller conspecifics, so that the rate at which fecundity increased with body size varied among years, and was highest when prey availability was greatest. Thus, the link between female body size and reproductive output varied among years, with climatic factors modifying the relative reproductive rates of larger (older) versus smaller (younger) animals within the keelback population.     

Maternal body volume constrains water uptake by lizard eggs in utero

1. Flexible shelled eggs of squamate reptiles normally take up substantial amounts of water, and swell accordingly, during development. However, most water uptake occurs after oviposition, beginning immediately or soon after oviposition, and water uptake is severely restricted in eggs that are retained in utero past the normal time of oviposition.
2. These observations suggest that some aspect of retention in the oviductal environment limits the amount of water eggs can absorb prior to oviposition.
3. This paper presents evidence, from two species of Sceloporus lizard, supporting the hypothesis that limited space within the mother's body cavity physically constrains the ability of eggs to expand, and thereby their ability to absorb water. When adjusted for maternal body size, the water content of a female's clutch of eggs is negatively correlated with the dry mass of her clutch (the space available in the body cavity is finite, and thus a greater dry mass content leaves less volume for water).
4. If such a constraint on water uptake is widespread, it can have important implications for our understanding of the evolution of viviparity, the costs of reproduction, and the determinants of reproductive output in squamate reptiles.     

Belly up: Reduced crevice accessibility as a cost of reproduction caused by increased girth in a rock‐using lizard

Costs of reproduction are any aspect of current reproduction that has the potential to reduce survivorship or reproductive output, and may include physiological costs or increased risks. Females of many species experience increased body mass, and increased girth, when gravid. Increased body mass reduces running speed and increases the cost of locomotion during pregnancy, but few studies have examined the cost of increased girth. If increased girth of gravid females reduces access to shelter from predators or the elements, increased girth could constitute a cost of reproduction. In the laboratory, we experimentally tested whether access to crevices was limited in viviparous, saxicolous female lizards (Eulamprus brachysoma), which use crevices for shelter, by measuring access to artificial crevices of known widths, and body height during and after pregnancy. Gravid E. brachysoma had significantly greater body height (11.2% on average), and as a result were forced to use significantly wider crevices (18.4% wider on average) than post‐parturition. Females with larger clutch sizes had wider mid‐bodies and required larger crevices. Control females, which were not gravid at either time of testing, showed no significant change in the size of crevice they could enter over time. If access to narrow crevices provides advantages such as protection from predators, or is important for thermoregulation, then gravid females may suffer a cost of reproduction because their access to narrower crevices is limited.     

Reproductive variation and adult size in two co-occurring grasshopper species

ABSTRACT. 1. Egg sizes and clutch sizes of the grasshoppers Chorthippus brunneus (Thunb.) and Myrmeleotettix maculatus (Thunb.) were compared among three years and among three sites less than 1.3 km apart. Relationships between these reproductive traits and date of egg laying, body size and body condition were sought.
2. M.maculatus , the smaller species, laid fewer but larger eggs; and only the eggs of this species showed significant differences between sites and years.
3. A negative correlation between egg size and number per clutch was evident between species and years, but generally not among sites and among individuals of a population.
4. However, a hidden negative correlation between egg size and number was uncovered within populations when the relationship was examined for females of a given mature weight.
5. Variation in the number of eggs per clutch was explained statistically by a positive relationship between female body weight and egg number. Also, both interpopulation and intrapopulation comparisons revealed that for M.maculatus , but not for C.brunneus , females with long hind femurs laid large eggs.     

Life-history variation in closely related generalist predators living in the same habitat: a case study with three Cyclosa spiders

1. Generalist predators sharing similar food resources and phenologies as well as having no competitive interactions are expected to have a similar life-history pattern, but some closely related web spiders show different life-history traits. The present paper clarifies possible selection pressures affecting life-history traits of the three coexisting Cyclosa spiders and explores the significance of the life-history variation.
2. Cyclosa argenteoalba had lower daily survival rate and higher growth rate, C. sedeculata had higher daily survival rate and lower growth rate, and C. octotuberculata showed intermediate levels. This implies that the selection pressures these spiders experience differ appreciably even in the same habitat.
3. The significance of the life-history characteristics of the three species was evaluated by general life-history theories. Cyclosa argenteoalba showed distinguishing reproductive traits: shorter time to maturation, larger reproductive effort, larger relative clutch size, decreased clutch size with the number of clutches, and smaller egg size. These characteristics may have evolved in response to the larger ratio of juvenile to adult survivorship. Cyclosa octotuberculata had a clutch size much larger than the other two species, but relative clutch sizes accounting for body size were similar between C. octotuberculata and C. sedeculata . Also, the two species showed a similar time to maturation despite having different selection pressures. Probably, higher growth rate compensates for lower survivorship, leading to the similarity in some reproductive traits.     

Interpreting reproductive allometry: Individual strategies of allocation explain size-dependent reproduction in plant populations

Size-dependent or allometric relationships between reproductive and vegetative size are extremely common in plant populations. Reproductive allometry where plant size differences are due to environmental variability has been interpreted both as an adaptive strategy of plant growth and allocation, and as the product of fixed developmental constraints. Patterns of development are crucial in defining reproductive allometry but development is not fixed across individuals. For example, environmental adversity (e.g. resource impoverishment) tends to favor reproduction at relatively small sizes – an adaptive response to environmental adversity. While small individuals may have lower reproductive output than large individuals, all plants should maximize their reproductive output and relative allocation to reproduction may be constant across sizes. Thus, where individual plants within a population initiate reproduction at different sizes, no significant reproductive allometry is an appropriate null expectation. Reproductive allometry occurs in plant populations where initiating reproduction at small sizes yields relatively high or low reproductive size at final development. Both of these outcomes are common in plant populations. Our interpretation of reproductive allometry combines previous adaptive and developmental constraint interpretations, and is the first to successfully explain the range of relationships in plant populations where relative allocation has been observed to increase, decrease or remain constant will increasing plant size.     

Patterns of reproductive effort in male and female shrubs of Oemleria cerasiformis: a 6-year study

1 We monitored flowering and fruiting of individual male and female plants of Oemleria cerasiformis over a 6-year period in a population in western Canada, and calculated fruit set (percentage of pistils maturing) and reproductive effort (RE) (gram of reproductive tissue per gram of leaf).
2 Over 6 years, male O. cerasiformis had on average much lower total RE, but much higher RE at flowering, than females.
3 In males, strong correlations between RE and light suggested that investment in reproduction was largely determined by light levels. There were strong positive correlations of RE between years, with no evidence of periodic fluctuations.
4 In females, in contrast to males, RE at flowering was not related to light. However, fruit set was strongly correlated with light. Flowering RE and fruit set were uncorrelated in females, indicating that these are affected by different factors.
5 Correlations of RE between years in females, although often significant, were lower than in males, indicating that RE fluctuates more between years in females than in males and may respond to past levels of RE. Flowering may reflect adjustments in response to past reproduction, or may be controlled by resources other than light. Fruit set was not significantly related to previous RE.
6 The greater total RE of females and their limited ability to adjust fruit set are probably major factors contributing to the greater mortality rates of females and the male-biased sex ratios in O. cerasiformis .     

Reproductive burden, locomotor performance, and the cost of reproduction in free ranging lizards

Abstract. A reduction in the locomotor capacity of gravid females is considered to be a cost of reproduction if it leads to an increased risk of mortality. In this study, we measured the change in endurance between gravid and postgravid female side-blotched lizards ( Uta stansburiana ) as a test of the cost of reproduction. We also altered reproductive investment in some females by direct ovarian manipulation (yolkectomy), which decreased reproductive burden by 30%. Regardless of experimental treatment, all females had lower endurance when gravid. Endurance was 28% lower in gravid females from the yolkectomy treatment and 31% lower in the unmanipulated females relative to postoviposition females. The experimental reduction in clutch mass resulted in a 21% increase in endurance of gravid yolkectomy females relative to control females. Postovipositional endurance was significantly higher in the yolkectomized females than unmanipulated females, which suggests that the cost of reproduction carries over to postoviposition performance. Unmanipulated females exhibited a significant negative association between endurance and size-specific burden. Endurance was not correlated with clutch size or size-specific burden in the yolkectomy females. Survivorship to the second clutch was higher in the yolkectomy females. The results from a logistic regression showed the probability of survival to the second clutch was significantly and positively associated with endurance after controlling for the effects of treatment. Our analyses demonstrated that the decrement in performance associated with current reproductive investment represents a cost of reproduction expressed as diminished locomotor performance and lowered survivorship to the next clutch.     

Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition

How much effort to expend in any one bout of reproduction is among the most important decisions made by an individual that breeds more than once. According to life-history theory, reproduction is costly, and individuals that invest too much in a given reproductive bout pay with reduced reproductive output in the future. Likewise, investing too little does not maximize reproductive potential. Because reproductive effort relative to output can vary with predictable and unpredictable challenges and opportunities, no single level of reproductive effort maximizes fitness. This leads to the prediction that individuals possessing behavioural mechanisms to buffer challenges and take advantage of opportunities would incur fitness benefits. Here, we review evidence in birds, primarily of altricial species, for the presence of at least two such mechanisms and evidence for and against the seasonal coordination of these mechanisms through seasonal changes in plasma concentrations of the pituitary hormone prolactin. First, the seasonal decline in clutch size of most bird species may partially offset a predictable seasonal decline in the reproductive value of offspring. Second, establishing a developmental sibling-hierarchy among offspring may hedge against unpredictable changes in resource availability and offspring viability or quality, and minimize energy expenditure in raising a brood. The hierarchy may be a product, in part, of the timing of incubation onset relative to clutch completion and the rate of yolk androgen deposition during the laying cycle. Because clutch size should influence the effects of both these traits on the developmental hierarchy, we predicted and describe evidence in some species that females adjust the timing of incubation onset and rate of yolk androgen deposition to match clutch size. Studies on domesticated precocial species reveal an inhibitory effect of the pituitary hormone prolactin on egg laying, suggesting a possible hormonal basis for the regulation of clutch size. Studies on the American kestrel (Falco sparverius) and other species suggest that the seasonal increase in plasma concentrations of prolactin may regulate both a seasonal advance in the timing of incubation onset and a seasonal increase in the rate of yolk androgen deposition. These observations, together with strong conceptual arguments published previously, raise the possibility that a single hormone, prolactin, functions as the basis of a common mechanism for the seasonal adjustment of reproductive effort. However, a role for prolactin in regulating clutch size in any species is not firmly established, and evidence from some species indicates that clutch size may not be coupled to the timing of incubation onset and rate of yolk androgen deposition. A dissociation between the regulation of clutch size and the regulation of incubation onset and yolk androgen deposition may enable an independent response to the predictable and unpredictable challenges and opportunities faced during reproduction.