Unraveling the complex phylogeographic history of freshwater fishes in Lower Central America: A study of the electric fish Brachyhypopomus occidentalis.

Lower Central America (LCA) has a complex biogeographic history shaped by the rise of the Isthmus of Panama and the global climatic oscillations of the Pleistocene. These events have been crucial in structuring biodiversity in LCA, but their consequences for the distribution and partitions of genetic diversity across the region remain to be elucidated. We combined complete mitochondrial genomes and nuclear ultraconserved elements (UCEs) to study the phylogeographic history and population genetic structure of the electric fish Brachyhypopomus occidentalis in LCA. Our results are consistent with the known phylogeographic history of B. occidentalis in LCA, but we update this history in several important ways that help illuminate the phylogeographic history of freshwater fishes in the region. We provide: i) support for three waves of colonization, two of which occurred prior to the final closure of the Panama Isthmus; ii) a more precise understanding of each colonization event, with evidence for a larger footprint of the first event, as well as genetic exchange across the continental divide in subsequent events; and iii) evidence for high levels of previously unrecognized population genetic structure across LCA. This updated model of colonization and diversification of B. occidentalis consists of three waves of dispersal and colonization, which triggered the evolution of geographic breaks in both nuclear and mitochondrial genomes across LCA. These processes are tightly linked to the dynamic uplift of the Isthmus, recent volcanic activity in the region, and the sea-level oscillations of the Pleistocene. These results improve previous phylogeographic inferences regarding the distribution and diversification of freshwater fishes in LCA, and generate testable hypotheses to guide future research exploring the factors shaping biodiversity in the region.

Temporally varying disruptive selection in the medium ground finch (Geospiza fortis).

Disruptive natural selection within populations exploiting different resources is considered to be a major driver of adaptive radiation and the production of biodiversity. Fitness functions, which describe the relationships between trait variation and fitness, can help to illuminate how this disruptive selection leads to population differentiation. However, a single fitness function represents only a particular selection regime over a single specified time period (often a single season or a year), and therefore might not capture longer-term dynamics. Here, we build a series of annual fitness functions that quantify the relationships between phenotype and apparent survival. These functions are based on a 9-year mark-recapture dataset of over 600 medium ground finches (Geospiza fortis) within a population bimodal for beak size. We then relate changes in the shape of these functions to climate variables. We find that disruptive selection between small and large beak morphotypes, as reported previously for 2 years, is present throughout the study period, but that the intensity of this selection varies in association with the harshness of environment. In particular, we find that disruptive selection was strongest when precipitation was high during the dry season of the previous year. Our results shed light on climatic factors associated with disruptive selection in Darwin's finches, and highlight the role of temporally varying fitness functions in modulating the extent of population differentiation.

Variable vision in variable environments: the visual system of an invasive cichlid (Cichla monoculus) in Lake Gatun, Panama.

An adaptive visual system is essential for organisms inhabiting new or changing light environments. The Panama Canal exhibits such variable environments owing to its anthropogenic origin and current human activities. Within the Panama Canal, Lake Gatun harbors several exotic fish species including the invasive peacock bass (Cichla monoculus), a predatory Amazonian cichlid. In this research, through spectral measurements and molecular and physiological experiments, we studied the visual system of C. monoculus and its adaptive capabilities. Our results suggest that (1) Lake Gatun is a highly variable environment, where light transmission changes throughout the canal waterway, and that (2) C. monoculus has several visual adaptations suited for this red-shifted light environment. Cichla monoculus filters short wavelengths (∼400 nm) from the environment through its ocular media and tunes its visual sensitivities to the available light through opsin gene expression. More importantly, based on shifts in spectral sensitivities of photoreceptors alone, and on transcriptome analysis, C. monoculus exhibits extreme intraspecific variation in the use of vitamin A1/A2 chromophore in their photoreceptors. Fish living in turbid water had higher proportions of vitamin A2, shifting sensitivities to longer wavelengths, than fish living in clear water. Furthermore, we also found variation in retinal transcriptomes, where fish from turbid and clear waters exhibited differentially expressed genes that vary greatly in their function. We suggest that this phenotypic plasticity has been key in the invasion success of C. monoculus.

Biological invasions alter the structure of a tropical freshwater food web.

Biological invasions are expected to alter food web structure, but there are limited empirical data directly comparing invaded versus uninvaded food webs, particularly in species-rich, tropical systems. We characterize for the first time the food web of Lake Gatun-a diverse and highly invaded tropical freshwater lake within the Panama Canal. We used stable isotope analysis to reconstruct the trophic structure of the fish community of Lake Gatun and to compare it to that of a minimally invaded reference lake, Lake Bayano. We found significant differences between the trophic structures of these two Neotropical lakes, notably that Lake Gatun's fish community was characterized by a longer food chain, greater isotopic diversity, a broader range of trophic positions and body sizes, and shifts in the isotopic positions of several native taxa relative to Lake Bayano. The degree of isotopic overlap between native and non-native trophic guilds in Lake Gatun was variable, with herbivores exhibiting the lowest (20%-29%) overlap and carnivores the greatest (81%-100%). Overall, our results provide some of the first empirical evidence for the ways in which multiple introduced and native species may partition isotopic space in a species-rich tropical freshwater food web.

The fitness landscape of a community of Darwin's finches.

Divergent natural selection should lead to adaptive radiation-that is, the rapid evolution of phenotypic and ecological diversity originating from a single clade. The drivers of adaptive radiation have often been conceptualized through the concept of "adaptive landscapes," yet formal empirical estimates of adaptive landscapes for natural adaptive radiations have proven elusive. Here, we use a 17-year dataset of Darwin's ground finches (Geospiza spp.) at an intensively studied site on Santa Cruz (Galápagos) to estimate individual apparent lifespan in relation to beak traits. We use these estimates to model a multi-species fitness landscape, which we also convert to a formal adaptive landscape. We then assess the correspondence between estimated fitness peaks and observed phenotypes for each of five phenotypic modes (G. fuliginosa, G. fortis [small and large morphotypes], G. magnirostris, and G. scandens). The fitness and adaptive landscapes show 5 and 4 peaks, respectively, and, as expected, the adaptive landscape was smoother than the fitness landscape. Each of the five phenotypic modes appeared reasonably close to the corresponding fitness peak, yet interesting deviations were also documented and examined. By estimating adaptive landscapes in an ongoing adaptive radiation, our study demonstrates their utility as a quantitative tool for exploring and predicting adaptive radiation.

The terroir of the finch: How spatial and temporal variation shapes phenotypic traits in DARWIN'S finches.

The term terroir is used in viticulture to emphasize how the biotic and abiotic characteristics of a local site influence grape physiology and thus the properties of wine. In ecology and evolution, such terroir (i.e., the effect of space or "site") is expected to play an important role in shaping phenotypic traits. Just how important is the pure spatial effect of terroir (e.g., differences between sites that persist across years) in comparison to temporal variation (e.g., differences between years that persist across sites), and the interaction between space and time (e.g., differences between sites change across years)? We answer this question by analyzing beak and body traits of 4388 medium ground finches (Geospiza fortis) collected across 10 years at three locations in Galápagos. Analyses of variance indicated that phenotypic variation was mostly explained by site for beak size (η 2 = 0.42) and body size (η 2 = 0.43), with a smaller contribution for beak shape (η 2 = 0.05) and body shape (η 2 = 0.12), but still higher compared to year and site-by-year effects. As such, the effect of terroir seems to be very strong in Darwin's finches, notwithstanding the oft-emphasized interannual variation. However, these results changed dramatically when we excluded data from Daphne Major, indicating that the strong effect of terroir was mostly driven by that particular population. These phenotypic results were largely paralleled in analyses of environmental variables (rainfall and vegetation indices) expected to shape terroir in this system. These findings affirm the evolutionary importance of terroir, while also revealing its dependence on other factors, such as geographical isolation.

100-year time series reveal little morphological change following impoundment and predator invasion in two Neotropical characids.

Human activities are dramatically altering ecosystems worldwide, often resulting in shifts in selection regimes. In response, natural populations sometimes undergo rapid phenotypic changes, which, if adaptive, can increase their probability of persistence. However, in many instances, populations fail to undergo any phenotypic change, which might indicate a variety of possibilities, including maladaptation. In freshwater ecosystems, the impoundment of rivers and the introduction of exotic species are among the leading threats to native fishes. We examined how the construction of the Panama Canal, which formed Lake Gatun, and the subsequent invasion of the predatory Cichla monoculus influenced the morphology of two native fishes: Astyanax ruberrimus and Roeboides spp. Using a 100-year time series, we studied variation in overall body shape over time (before vs. after impoundment and invasion) as well as across space (between an invaded and an uninvaded reservoir). In addition, we examined variation in linear morphological traits associated with swim performance and predator detection/avoidance. Notwithstanding a few significant changes in particular traits in particular comparisons, we found only limited evidence for morphological change associated with these two stressors. Most observed changes were subtle, and tended to be site- and species-specific. The lack of a strong morphological response to these stressors, coupled with dramatic population declines in both species, suggests they may be maladapted to the anthropogenically perturbed environment of Lake Gatun, but direct measures of fitness would be needed to test this. In general, our results suggest that morphological responses to anthropogenic disturbances can be very limited and, when they do occur, are often complex and context-dependent.

Urbanization erodes niche segregation in Darwin's finches.

Urbanization is influencing patterns of biological evolution in ways that are only beginning to be explored. One potential effect of urbanization is in modifying ecological resource distributions that underlie niche differences and that thus promote and maintain species diversification. Few studies have assessed such modifications, or their potential evolutionary consequences, in the context of ongoing adaptive radiation. We study this effect in Darwin's finches on the Galápagos Islands, by quantifying feeding preferences and diet niche partitioning across sites with different degrees of urbanization. We found higher finch density in urban sites and that feeding preferences and diets at urban sites skew heavily toward human food items. Furthermore, we show that finches at urban sites appear to be accustomed to the presence of people, compared with birds at sites with few people. In addition, we found that human behavior via the tendency to feed birds at non-urban but tourist sites is likely an important driver of finch preferences for human foods. Site differences in diet and feeding behavior have resulted in larger niche breadth within finch species and wider niche overlap between species at the urban sites. Both factors effectively minimize niche differences that would otherwise facilitate interspecies coexistence. These findings suggest that both human behavior and ongoing urbanization in Galápagos are starting to erode ecological differences that promote and maintain adaptive radiation in Darwin's finches. Smoothing of adaptive landscapes underlying diversification represents a potentially important yet underappreciated consequence of urbanization. Overall, our findings accentuate the fragility of the initial stages of adaptive radiation in Darwin's finches and raise concerns about the fate of the Galápagos ecosystems in the face of increasing urbanization.

Low Predictability of Colour Polymorphism in Introduced Guppy (Poecilia reticulata) Populations in Panama.

Colour polymorphism is a recurrent feature of natural populations, and its maintenance has been studied in a range of taxa in their native ranges. However, less is known about whether (and how) colour polymorphism is maintained when populations are removed from their native environments, as in the case of introduced species. We here address this issue by analyzing variation in colour patterns in recently-discovered introduced populations of the guppy (Poecilia reticulata) in Panama. Specifically, we use classic colour analysis to estimate variation in the number and the relative area of different colour spots across low predation sites in the introduced Panamanian range of the species. We then compare this variation to that found in the native range of the species under low- and high predation regimes. We found aspects of the colour pattern that were both consistent and inconsistent with the classical paradigm of colour evolution in guppies. On one hand, the same colours that dominated in native populations (orange, iridescent and black) were also the most dominant in the introduced populations in Panama. On the other, there were no clear differences between either introduced-low and native low- and high predation populations. Our results are therefore only partially consistent with the traditional role of female preference in the absence of predators, and suggest that additional factors could influence colour patterns when populations are removed from their native environments. Future research on the interaction between female preference and environmental variability (e.g. multifarious selection), could help understand adaptive variation in this widely-introduced species, and the contexts under which variation in adaptive traits parallels (or not) variation in the native range.

Life history change in response to fishing and an introduced predator in the East African cyprinid Rastrineobola argentea.

Fishing and introduced species are among the most important stressors affecting freshwaters and can also be strong selective agents. We examined the combined effects of commercial fishing and an introduced predator (Nile perch, Lates niloticus) on life history traits in an African cyprinid fish (Rastrineobola argentea) native to the Lake Victoria basin in East Africa. To understand whether these two stressors have driven shifts in life history traits of R. argentea, we tested for associations between life history phenotypes and the presence/absence of stressors both spatially (across 10 Ugandan lakes) and temporally (over four decades in Lake Victoria). Overall, introduced Nile perch and fishing tended to be associated with a suite of life history responses in R. argentea, including: decreased body size, maturation at smaller sizes, and increased reproductive effort (larger eggs; and higher relative fecundity, clutch volume, and ovary weight). This is one of the first well-documented examples of fisheries-induced phenotypic change in a tropical, freshwater stock; the magnitude of which raises some concerns for the long-term sustainability of this fishery, now the most important (by mass) in Lake Victoria.

Life history change in commercially exploited fish stocks: an analysis of trends across studies.

Age and size at maturation have declined dramatically in many commercial fish stocks over the past few decades - changes that have been widely attributed to fishing pressure. We performed an analysis of such trends across multiple studies, to test for the consistency of life history changes under fishing, and for their association with the intensity of exploitation (fishing mortality rate). We analyzed 143 time series from 37 commercial fish stocks, the majority of which originated from the North Atlantic. Rates of phenotypic change were calculated for two traditional maturation indices (length and age at 50% maturity), as well as for probabilistic maturation reaction norms (PMRNs). We found that all three indices declined in heavily exploited populations, and at a rate that was strongly correlated with the intensity of fishing (for length at 50% maturity and PMRNs). These results support previous assertions that fishing pressure is playing a major role in the life history changes observed in commercial fish stocks. Rates of change were as strong for PMRNs as for age and size at 50% maturity, which is consistent with the hypothesis that fishing-induced phenotypic changes can sometimes have a genetic basis.