Female Festive Anole (photo: Ambika Kamath)

The evolution of reproductive strategies is an interplay between phylogenetic constraints (i.e. restrictions determined by the evolutionary history of that organism) and local conditions. Organisms adapt their reproductive physiology to their environment in ways that maximize fitness; however, this occurs within the context of evolutionary history (e.g. income vs. capital breeders).  When environments are seasonal, selection favors individuals that align changes in key reproductive traits (e.g., egg size, clutch size) with seasonal shifts in habitat quality. For example, some species of aphids switch from asexual to sexual reproduction in the fall of each year because offspring produced via sexual reproduction (i.e. genetic recombination) are more likely to survive the winter. Seasonal shifts in reproduction have been observed in a variety of taxa (e.g. birds, mammals, frogs, lizards, spiders).

In two previous papers, the Warner Lab demonstrated that brown anoles (Genus-pending sagrei) in Florida, exhibit seasonal shifts in reproduction (Mitchell et al 2018; Pearson & Warner 2018): females shifts from producing many, relatively small offspring early in the year to producing fewer, relatively large offspring late in the year. Pearson and Warner (2018) also demonstrated that anoles that hatch early in the season (March – May) are more likely to survive through winter than those that hatch later (July-August). Thus, the observed shift in reproduction appears to be an evolved response to the seasonal decline in offspring habitat. This shift in reproduction, however, may depend on environmental factors that are also subject to temporal changes (e.g., food abundance).

In a new paper (Hall et al 2018) published in Physiological and Biochemical Zoology, we demonstrate how prey abundance modifies seasonal changes in key reproductive traits for brown anoles. We bred lizards in controlled laboratory conditions across the length of a full reproductive season and manipulated the availability of food by providing some breeding pairs high prey availability and some low. Halfway through the season, we switched half of the breeding pairs to the opposite treatment. We measured growth of male and female lizards as well as latency to oviposit, fecundity, egg size, egg content (yolk, water, shell mass), and egg quality (steroid hormones, yolk caloric content) over this period.

Higher prey availability enhanced lizard growth and some key reproductive traits (egg size, fecundity), but not others (egg content and quality). Notably, egg quality seems unaffected by diet. This is probably because there is some minimum provisioning that is necessary to produce a viable egg. Thus, females on a low-calorie diet will sacrifice the number of eggs produced and not the quality; however, increased food supply will be primarily used to increase fecundity.

We also found that seasonal patterns of reproduction were modified by prey treatment in ways that have consequences for offspring survival (Fig 1). When prey was abundant, egg production peaked relatively early in the season and egg size increased through time; however, when prey availability was low, egg production was chronically low and egg size declined through time. Late-produced offspring are at a disadvantage because they have to compete with larger, established offspring that hatched earlier in the year. A low calorie diet prevents females from providing late-season offspring with the extra provisions they need to compensate for hatching late.

Figure 1. Egg production of brown anoles provided with a) continuously high prey availability; b) high prey availability switched to low; c) continuously low prey availability; d) low prey availability switched to high. The vertical dotted line represents the point in the experiment when the diets were changed for groups b and d.

Figure 2. The relationships between latency to oviposit and a) prey treatment and b) pre-season body condition. Dark bar/circles show the high prey treatment and white bar/circles show the low prey treatment.

Not shockingly, when the diets were switched halfway through the season (high prey switched to low or the reverse; Fig 1) females responded immediately to the new diet. This would suggest that anoles are primarily income breeders that utilize energy intake to fuel reproduction. However, we know that income and capital breeding is a continuum and many reptiles utilize both for reproduction. We also found that females with a relatively high body condition at the beginning of the experiment start laying eggs earlier than those with poorer body condition (Fig 2). These measures of condition were taken prior to the onset of reproduction and couldn’t have been confounded by the presence/absence of oviductal eggs. Like many reptiles, pre-season body condition (i.e., fat reserves) may play an important role in the initiation of reproduction (vitellogenesis) for anoles; however, once reproduction starts, income is likely the primary determinant of fecundity.

Our results demonstrate that seasonal changes in anole reproduction are dependent on fluctuations in local environmental conditions.

Joshua Hall
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