A central issue in ecology is understanding patterns of distribution and abundance, the selective pressures underlying these patterns, and their evolutionary consequences. The physical environment has a major influence on the ecology of organisms; and for fishes, availability of dissolved oxygen (DO) is one factor that can limit habitat quality. Despite great interest in evolution of adaptations to deoxygenation (e.g., development of air-breathing organs), the role of DO in maintenance of fish faunal and diversity remains relatively unexplored. Hypoxic (oxygen-scarce) waters may serve as barriers to fish movement, biofilters, or refuges depending on the relative tolerance of fishes. Increasing levels of hypoxia associated with anthropogenic disturbance may therefore alter ecological dynamics of fish communities and contribute to microevolutionary change.
n our studies of respiratory ecology, we are using a combination of field studies in Uganda and laboratory studies at McGill University to explore the role of dissolved oxygen (DO) as a divergent selective factor contributing to inter- and intrademic variation in freshwater fishes. Our studies of East African fishes have demonstrated that alternative DO environments provide a strong predictor of intraspecific variation, particularly with respect to respiratory traits (e.g., gill size, critical oxygen tension) and associated characters (Chapman, 2006). We began our study of interdemic variation by quantifying the relationship between total gill filament length (TGFL) and DO for the cyprinid Barbus neumayeri from six sites in the Mpanga River drainage of Uganda. TGFL increased as DO decreased, indicating interdemic variation in a morphological trait that correlates with oxygen availability (Chapman et al., 1999). Further study revealed differences in respiratory behavior (Olowo and Chapman, 1996), hematocrit (Martinez et al., 2004), lactate dehydrogenase (Martinez et al., 2004), and metabolic rate and critical tension (Chapman, 2006) between B. neumayeri from swamps and from open waters.
In recent interdemic comparisons, we found total gill size (surface area and or total filament length) to be larger in swamp-dwelling populations of the African mormyrids Gnathonemus victoriae and Petrocephalus catostoma (Chapman and Hulen, 2001), the African cichlids Pseudocrenilabrus multicolor victoriae (Chapman et al., 2000) and Astatoreochromis alluaudi (Chapman et al, 2007), the N. American poeciliid Poecilia latipinna (Timmerman and Chapman, 2004), and the air-breathing African catfish Clarias liocephalus (McCue, 2001) relative to open-water populations. Given the widespread occurrence of oxygen scarcity in aquatic systems, and increasing levels of hypoxia associated with anthropogenic influence, microevolution in response to hypoxic stress may be a frequent phenomenon in nature.
An important step in documenting divergent natural selection is to explain why alternative phenotypes persist in different environments. Performance of different phenotypes between alternative habitats can be used to detect fitness trade-offs. In fishes, trade-offs between feeding and respiratory structures seem likely because of their compact, laterally compressed head morphology, and our studies suggest that such trade-offs do occur. For example, we demonstrated that adaptive change in gill size (large gills) in fish from hypoxic waters correlates with reduced size of key trophic muscles and feeding performance relative to small-gilled conspecifics (Chapman et al., 2000, Schaack and Chapman, 2003). These trade-offs may lead to fitness costs in the field that impose habitat-specific selection pressures on dispersers (Chapman et al., 1999). This could lead to immigrant inviability and directly reduce gene flow.
Clearly hypoxic stress may influence phenotypes directly, but also indirectly via trait correlations and interactions with other environmental variables. A next step in understanding morphological response to hypoxic stress is to explore the interaction of other environmental characters that impact fish morphology and may influence morphological response to hypoxia. For example, we have shown that several fishes have larger gills in more hypoxic waters (a shared response), but the effect of a larger branchial basket on streamline may differ depending on whether the fish is in flowing or stagnant water. Thus, nonrespiratory factors may influence extent of divergence in respiratory characters and vice versa.
Two good candidates for tradeoffs between gills and non-respiratory structures are hydrodynamic constraints and constraints due to durophagy (hard foods). In a recent study using nine populations of B. neumayeri, we employed path analysis to examine direct, indirect, and total effects of two environmental variables, water flow and dissolved oxygen, on several morphological traits (Langerhans, Chapman, and DeWitt, 2007).
With our background of studies on interdemic variation in the respiratory ecology of East African fishes, we are now addressing a series of objectives that will advance our understanding of the nature of direct and indirect forms of divergent natural selection in a novel tractable system – divergent oxygen environments. These studies are collaborative in nature (Dr. Tom Dewitt (Texas A & M), Dr. Frietson Galis (Leiden University), Brian Langerhans (North Carolina State University), Dr. James Albert, (University of Louisiana at Lafayette), will facilitate training both nationally and internationally, and stimulate continued collateral work in wetlands biology, aquatic conservation, and fisheries in Uganda.
Our objectives are to (1) identify key predictors of dissolved oxygen (DO) variation in the field across scales of time and space, (2) define and quantify both the shared and unique aspects of morpho-physiological diversification of multiple fish species in response to DO gradients, (3) document performance tradeoffs in the laboratory, (4) explore fitness tradeoffs in the field, (5) quantify the degree to which developmental plasticity and canalized genetic differences contribute to observed patterns using common garden rearing experiments, and (6) explore indirect tradeoffs associated with DO and two other diversifying agents (food and water current).
To expand the phylogenetic and geographic scope of our exploration of divergence across oxygen gradients, we are also collaborating with Dr. William Crampton (University of Central Florida) on a project that quantifies inter- and intraspecific variation in the respiratory morphology of Amazon gymnotid (electric) fishes of the genus Brachyhypopomus.
In addition, we are adding a critical new dimension to our studies of respiratory ecology by moving from the organismal to the biochemical level to examine the biochemical bases of hypoxia tolerance. This joint program with Dr. Bernard Rees (University of New Orleans), Dr. Mery Martinez (Laurentian University) to determine the level of interdemic variation in tissue metabolic capacities in field populations of African fishes and to evaluate the degree to which interdemic variation in the biochemical response to hypoxia is the result of phenotypic plasticity.