Studies of Ecology and Morphology in the plethodontid salamander genus Batrachoseps

by

Christopher James Evelyn

Evolution of interspecific morphological diversity within a clade is one of the fundamental patterns studied in evolutionary biology. These morphological differences may reflect adaptation to different environmental conditions and influence patterns across biogeographical spatial scales and macroevolutionary time scales. Using a multivariate measure of morphological shape and a well-studied phylogenetic hypothesis for the plethodontid salamander genus Batrachoseps, I revealed the strong correlation between morphology and species range size, and tested ecological hypotheses that might explain this relationship. Morphological evolution in Batrachoseps can be generally described as variation on the theme of elongation, a pattern also seen in several families of lizards such as Scincidae and Gymnophthalmidae. In Batrachoseps the most elongate forms appear wormlike with highly reduced limbs. Generalized forms of Batrachoseps are similar in proportion to other small salamanders in the family Plethodontidae, such as Plethodon.

To investigate whether morphological differences reflect a difference in habitat use, a pair of closely related species were studied where their ranges overlap (Chapter 1). Broad partitioning of habitat was the rule with the wormlike B. nigriventris occupying low to middle elevation sites (600-1200 meters) and the more generalized B. stebbinsi occupying middle to high elevation sites (1100-1800 meters). These species showed considerable overlap in their use of microhabitat in terms of temperature, moisture, and cover objects. Despite their ecological similarity B. nigriventris has a much larger species range (34,000 km2) than B. stebbinsi (1,300 km2). This is consistent with the strong correlation between evolution of species range size and evolution of elongation in Batrachoseps (Chapter 2). Species range size in wormlike species is an order of magnitude larger than more generalized forms. Overall the evolution of elongation in Batrachoseps is a strong and significant predictor of the evolution of large range size. This pattern is not achieved by wormlike forms evolving to occupy wider elevational ranges or more abundant low elevation habitat. Large range size is an important metric for predicting the probability of species extinction. Finding traits that predict extinction is of central interest to the study of conservation biology and macroevolution.

A previously proposed hypothesis posited that evolution of wormlike morphology in Batrachoseps is a response to dry, seasonal, and unpredictable precipitation patterns. Individuals with small diameters could more easily retreat to subsurface refugia when surface conditions are inhospitable. These small salamanders depend upon seasonal precipitation events for surface activity to carry out basic life history activities. When surface conditions are moist Batrachoseps feed, breed, and re-hydrate after long periods of inactivity below the surface. I found a strong correlation between evolution of wormlike morphology and evolution to persist in more seasonal habitats (Chapter 3). Dry season precipitation and precipitation seasonality were significantly correlated with morphological evolution in Batrachoseps. This result suggests that wormlike morphology is advantageous in habitats where food resources and mating opportunities are only available periodically. All Batrachoseps appear to occupy similar microhabitat but persistence in highly seasonal habitats with low levels of dry season precipitation is associated with evolution of elongate morphology.

The introduction and spread of novel pathogens is an increasingly important contributor to biodiversity loss, and Batrachochytrium dendrobatidis (Bd), the causative agent of the deadly amphibian disease chytridiomycosis, has led to the declines or extinctions of many amphibians globally. Repatriation programs are increasing in response to species extirpations; however, a prerequisite to these programs is an understanding of the causative factors in declines. The foothill yellow-legged frog (Rana boylii) was enigmatically extirpated from the southern California portion of its range between the late 1960s and the mid-1970s. Little is known about the cause of this rapid, localized extinction event, R. boylii’s Bd susceptibility, the impact of Bd on extant R. boylii populations, or the history and current status of Bd in amphibian populations in southern California. I tested the hypothesis that Bd could have played an important role in the rapid extirpation of R. boylii from southern California through field surveys, laboratory experiments, interviews, and museum specimen sampling. I found that where the species is extant in central California, it is lethally susceptible to chytridiomycosis, and that infection is related to the presence of non-native American bullfrogs. I optimized methods to detect Bd DNA from formalin-fixed museum specimens using real-time quantitative polymerase chain reaction (qPCR), and found that both DNA extraction method and the pathogen load of frogs prior to formalin fixation are important predictors of successful Bd DNA detection. Finally, using an interdisciplinary approach that combined museum specimen sampling, interviews, and field notes, I examined the historical prevalence of Bd and abundance of R. boylii in southern California, and the timing of R. boylii’s extirpation. I found that Bd prevalence increased in the mid-to-late 20th century and coincided with R. boylii’s rapid decline from the region. This work reveals new insights into the current and historical role of chytridiomycosis in California amphibian declines and can serve to inform future R. boylii reintroduction efforts.