Robin M. Andrews

I present the results of 50 yr (1971–2020) of annual censuses of Anolis apletophallus on Barro Colorado Island, Panama. The main objectives were to assess why abundance in end-of-the-year censuses varied substantially from year to year and why it declined over time. Abundance was negatively correlated with annual rainfall, 90% of which occurs in the wet season when eggs are laid. Lizard abundance is indirectly linked to rainfall through the interaction between Anolis eggs and their major predator, Solenopsis ants. More eggs are killed by ants when rainfall is relatively high because ants are more active and encounter more eggs than when rainfall is relatively low. While rainfall accounts for variability in abundance, it has not changed over time and thus may not account for the overall decline in abundance. Model selection of AICc analyses identified two other factors correlated with abundance. Abundance was positively correlated with the Southern Oscillation Index (SOI) lagged by 1 yr. High SOI (and high abundance) is associated with cool and wet La Niña conditions and low values with dry and warm El Niño conditions. The prediction that low abundance is associated with dry and warm El Niño conditions (low SOI) conflicts with the negative correlation between abundance and rainfall where low abundance is associated with high rainfall. Moreover, abundance was negatively correlated with Tmin (minimum annual temperature). The mechanism by which increasing Tmin during the census period is linked to declining abundance is unknown. Three climatic factors are correlated with lizard abundance, but none of them explain why abundance has declined. A third objective was to examine the relationship between species richness and species dominance of Anolis communities with respect to rainfall patterns. Tropical forests typically have a maximal richness of 7–8 species. Our study sites in Panama have high species richness, but Anolis apletophallus individuals made up ≥96% of all records, an unexpected level of species dominance. Comparisons among sites suggest that the number of Anolis species in a community is related to annual rainfall, and dominance is related to seasonality of rainfall. Dry forests have few Anolis species and wet forests have as many as 7–8 species. Forests with short wet seasons (months with >100 mm rainfall) have a high likelihood that individuals of one species will dominate the community.

Highly mineralized rigid‐shelled eggs characterize one lineage of gekkotans. In contrast, poorly mineralized flexible‐shelled eggs characterize basal lineages of gekkotans and all other squamates. Low oxygen permeability of rigid‐shelled eggs is associated with small eggs and hatchlings, and long incubation lengths compared to flexible‐shelled gekkotan eggs. These features represent a demographic cost for species with rigid‐shelled eggs. This cost is offset, at least in part, because mortality due to desiccation and predation is reduced for rigid‐shelled eggs relative to flexible‐shelled eggs. Developmental traits may also compensate for the low oxygen permeability of rigid‐shelled eggs. Oviposition, for example, occurs at earlier developmental stages for gekkotans with rigid‐ versus flexible‐shelled eggs. Such early oviposition facilitates development because eggs move from the relatively hypoxic oviduct to the much better oxygenated nest environment. In this study, I tested the hypothesis that the growth of the yolk sac (YS) and chorioallantoic membrane (CAM) of gekkotans with rigid‐shelled eggs is initiated and completed earlier than those of gekkotans with flexible‐shelled eggs. I measured the surface area of eggs covered by the YS and CAM from oviposition to hatching and determined which of four nonlinear models provide the best fit for growth curves. I also compiled a data set on embryonic metabolism of gekkotans and other lizards in order to place growth of the YS and CAM in the context of energy utilization of lizard embryos overall. Growth of the YS and CAM of gekkotans with rigid‐shelled eggs is accelerated relative to that of gekkotans with flexible‐shelled eggs and may serve to separate the cost of YS and CAM development from that of the embryo itself. Adaptive variation in YS and CAM development may extend to birds, crocodilians, and turtles as they also exhibit life history variation that affects oxygen availability to embryos during development.

Limb reduction among squamate clades is common; limbless (forelimbs, hindlimbs, or both) forms have had at least 25 independent origins among snakes and lizards. The general evolutionary pattern is the gradual loss of limb elements proceeding from the toes to the shoulder or hip. In contrast, forelimbs are not known to have ever existed in snakes. Forelimbs are not known for either stem or crown snakes; snake fossils lack forelimbs and the embryos of modern snakes lack the signaling pathways that initiate forelimb development. Both fossil and developmental data thus imply an abrupt loss of forelimbs. In contrast, the well-developed hindlimbs of the oldest fossil snakes and vestigial hindlimbs of some basal clades of modern snakes imply the historical presence of hindlimbs, and their gradual reduction during snake evolution. In contrast, observations on limb-reduced lizards are in accord with gradual reduction of both fore- and hindlimbs; embryos of even limbless species initiate limb development. The question then arises, have any clades of limbless lizards become limbless abruptly, as have snakes? To address this question, I examined limb development in the family Pygopodidae. Like basal snakes, pygopodids are characterized by the absence of forelimbs and by vestigial hindlimbs. My observations on the development of forelimb buds in Delma molleri support gradual limb reduction, as do observations on other limbless lizards. Nonetheless, many clades of limbless lizards are yet to be studied and hence provide a wealth of opportunities to address modes of limb reduction and loss in squamate reptiles.

This research perspective focuses on three of the disciplinary areas that have engaged my interest as a professional biologist. My research first focused on life history evolution, but it expanded to include the evolution of viviparity, and developmental biology. My subjects are squamate reptiles, although I do hands-on research largely with lizards. A common theme of the research that I discuss here is the role of eggs and embryos in ecological and evolutionary studies and why that role may be critical to the resolution of important biological problems. In this perspective, I summarize highlights of my major research projects since 1971: 1) life history evolution of West Indian island and mainland Anolis lizards; 2) long-term studies on the demography and egg survival of a small, r-selected Panamanian anole; 3) ecological and physiological studies on the transition between oviparity and viviparity in Sceloporus; 4) costs and benefits of the novel rigid-shelled egg of gekkotan lizards; and 5) embryonic adaptations to low oxygen availability in rigid-shelled eggs of gekkotan lizards. I put these projects in the context of my own developmental trajectory as a biologist; my research has shifted from population biology to embryonic development without breaking the connection between these seemingly disparate disciplines.

Embryonic environments affect a range of phenotypic traits including sex and reproductive success. I determined (1) how the interaction between incubation temperature and egg size affects sex allocation of Chamaeleo calyptratus and (2) how incubation temperature and maternal parent (clutch) affect water uptake by eggs and body size, growth, and climbing speed of hatchlings and juveniles. Eggs from five clutches were exposed to five temperature treatments with clutches replicated within and among treatments. Temperature affected sex, but only when egg size was included as a factor in analyses. At intermediate (28°C) temperatures, daughters were more likely to be produced from large eggs and sons more likely to be produced from small eggs, while at 25 and 30°C, the pattern of sex allocation was reversed. Temperature and clutch affected water uptake and body size. Nonetheless, the direction of temperature and clutch effects on water uptake by eggs and on the size of hatchlings were not the same and the direction of temperature effects on body sizes of hatchlings and juveniles differed as well. Clutch affected hatchling size but not juvenile size and growth rate. Clutch, but not incubation temperature, affected climbing speed, but the fastest hatchlings were not from the same clutches as the fastest juveniles. The independent effects of incubation temperature and clutch indicate that hatchling phenotypes are influenced largely by conditions experienced during incubation, while juvenile phenotypes are influenced largely by conditions experienced in the rearing environment.

The rate of anthropogenic habitat conversion often exceeds the rate of natural ecological and evolutionary processes, which sometimes creates mismatches between environmental cues and adaptive behaviors. In numerous species of aquatic turtles, nest site selection is primarily based on cues related to high solar exposure, which leads females to select sites where humans have disturbed habitat. These disturbed sites are often contaminated by pollutants, such as mercury. Despite the fact that anthropogenic disturbances often co‐occur, few studies have examined the interactive influence of major global changes on animal development. Using Chelydra serpentina, we investigated the individual and interactive effects of crop agriculture and mercury pollution on hatch success and offspring phenotype. We hypothesized that following nesting, rapid crop growth would shade and cool nests in agricultural fields and subsequently negatively impact embryonic development. Agricultural and control nests were similar in temperature at the time of oviposition, but temperatures diverged as crops grew: agricultural nests averaged 2.5°C cooler than control nests over the course of incubation. In laboratory and field experiments, we found that turtles incubated under agricultural thermal regimens took longer to hatch, hatched at smaller body sizes, lost more mass, and had lower posthatching growth rates. Additionally, thermal conditions associated with agricultural land use interacted with mercury contamination to decrease hatching success. To our knowledge, this is the first documentation of negative interactive effects of mercury pollution and habitat quality on early vertebrate development and highlights the importance of examining the combined influence of anthropogenic global changes on organisms.

Varanus rosenbergi females oviposit in nests excavated in termite mounds in summer, and hatching occurs the following spring after a seven-month incubation period. In this study, we characterized developmental features associated with the prolonged incubation of this species at Kangaroo Island in South Australia. Oviposition occurs shortly after limb buds have formed, and the subsequent pattern of organogenesis is similar to that of other lizards. Survival of eggs incubated at constant temperatures ranging from 26–33°C was 89–100%, whereas survival at 24°C and at 35°C was 0 and 14%, respectively. During the incubation period, mean ambient temperature at Kangaroo Island (14–15°C) is too low for successful reproduction, whereas mean temperatures in termite mounds (27–37°C) are substantially warmer and similar to the estimated mean incubation temperature (26–27°C). Therefore, successful reproduction by V. rosenbergi in southern Australia may be contingent on nesting in termitaria. Varanids, in gener...

The majority of lizards and snakes lay flexible-shelled eggs with high water vapor permeability and which absorb water during incubation and increase in mass, volume, and surface area (water uptake is necessary for successful embryonic development). In contrast, one clade of gekkotans lay rigid-shelled eggs with low permeability which, like bird eggs, lose water during incubation and incubate successfully under low moisture conditions. Anecdotal accounts suggest that eggs of some New Caledonian diplodactylids, a family of gekkotans characterized by flexible-shelled eggs, are ‘hard-shelled.' I made observations on the eggs of Correlophus ciliatus (= Rhacodactylus ciliatus) to test the idea that New Caledonian diplodactylid eggs exhibit features unlike those of other squamates that lay flexible-shelled eggs. I found that C. ciliatus eggs are flexible-shelled; they have relatively high water vapor permeability and they increase in mass during incubation as the result of water uptake. Nonetheless, egg characteristics fall outside the range of values observed for squamates that lay flexible-shelled eggs. While C. ciliatus eggs increase in mass (as expected of flexible-shelled eggs), the magnitude of increase is substantially lower than in eggs of other squamates. Moreover, water vapor permeability of C. ciliatus eggs is about 40% that of flexible-shelled eggs of the same mass. Therefore, shell characteristics appear to be transitional between flexible- and rigid-shelled eggs. This suggests that the diplodactylid geckos of New Caledonia may provide a unique opportunity to explore the nature of the evolutionary transition between two disparate shell types.

In many respects, reptile hatchlings are fully functional, albeit miniature, adults. This means that the adult morphology must emerge during embryonic development. This insight emphasizes the connection between the mechanisms that generate phenotypic variation during embryonic development and the action of selection on post-hatching individuals. To determine when species-specific differences in limb and tail lengths emerge during embryonic development, we compared allometric patterns of early limb growth of four distantly related species of lizards. The major questions addressed were whether early embryonic limb and tail growth is characterized by the gradual (continuous allometry) or by the abrupt emergence (transpositional allometry) of size differences among species. Our observations supported transpositional allometry of both limbs and tails. Species-specific differences in limb and tail length were exhibited when limb and tail buds first protruded from the body wall. Genes known to be associated with early limb development of tetrapods are obvious targets for studies on the genetic mechanisms that determine interspecific differences in relative limb length. Broadly comparative studies of gene regulation would facilitate understanding of the mechanisms underlying adaptive variation in limb size, including limb reduction and loss, of squamate reptiles.

The majority of lizards and snakes produce permeable parchment‐shelled eggs that require high moisture conditions for successful embryonic development. One clade of gekkotan lizards is an exception; females produce relatively impermeable rigid‐shelled eggs that normally incubate successfully under low moisture conditions. I tested the hypothesis that the rigid‐shell increases egg survival during incubation, but only under low moisture conditions. To test this hypothesis, I incubated rigid‐shelled eggs of Chondrodactylus turneri under low and under high moisture conditions. Eggs were incubated with parchment‐shelled eggs of Eublepharis macularius to insure that incubation conditions were suitable for parchment‐shelled eggs. Chondrodactylus turneri eggs had very high survival (>90%) when they were incubated under low moisture conditions. In contrast, eggs incubated under high moisture conditions had low survival overall, and lower survival than those of the parchment‐shelled eggs of E. macularius. Mortality of C. turneri and E. macularius eggs incubated under high moisture conditions was the result of fungal infection, a common source of egg mortality for squamates under laboratory and field conditions. These observations document high survival of rigid‐shelled eggs under low moisture conditions because eggs escape from fungal infection. Highly mineralized rigid shells also make egg survival independent of moisture availability and may also provide protection from small invertebrates in nature. Enhanced egg survival could thus compensate for the low reproductive output of gekkotans that produce rigid‐shelled eggs. J. Exp. Zool. 323A: 607–615, 2015.