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.

Asymmetric Isolation and the Evolution of Behaviors Influencing Dispersal: Rheotaxis of Guppies above Waterfalls.

Populations that are asymmetrically isolated, such as above waterfalls, can sometimes export emigrants in a direction from which they do not receive immigrants, and thus provide an excellent opportunity to study the evolution of dispersal traits. We investigated the rheotaxis of guppies above barrier waterfalls in the Aripo and Turure rivers in Trinidad-the later having been introduced in 1957 from a below-waterfall population in another drainage. We predicted that, as a result of strong selection against downstream emigration, both of these above-waterfall populations should show strong positive rheotaxis. Matching these expectations, both populations expressed high levels of positive rheotaxis, possibly reflecting contemporary (rapid) evolution in the introduced Turure population. However, the two populations used different behaviors to achieve the same performance of strong positive rheotaxis, as has been predicted in the case of multiple potential evolutionary solutions to the same functional challenge (i.e., "many-to-one mapping"). By contrast, we did not find any difference in rheotactic behavior above versus below waterfalls on a small scale within either river, suggesting constraints on adaptive divergence on such scales.

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.

Habitat filtering not dispersal limitation shapes oceanic island floras: species assembly of the Galápagos archipelago.

Remote locations, such as oceanic islands, typically harbour relatively few species, some of which go on to generate endemic radiations. Species colonising these locations tend to be a non-random subset from source communities, which is thought to reflect dispersal limitation. However, non-random colonisation could also result from habitat filtering, whereby only a few continental species can become established. We evaluate the imprints of these processes on the Galápagos flora by analysing a comprehensive regional phylogeny for ~ 39 000 species alongside information on dispersal strategies and climatic suitability. We found that habitat filtering was more important than dispersal limitation in determining species composition. This finding may help explain why adaptive radiation is common on oceanic archipelagoes - because colonising species can be relatively poor dispersers with specific niche requirements. We suggest that the standard assumption that plant communities in remote locations are primarily shaped by dispersal limitation deserves reconsideration.

Host preference of an introduced 'generalist' parasite for a non-native host.

Parasites can invade new ecosystems if they are introduced with their native hosts or if they successfully infect and colonise new hosts upon arrival. Here, we ask to what extent an introduced parasite demonstrates specialisation among novel host species. Infection surveys across three field sites in Gatun Lake, Panama, revealed that the invasive peacock bass, Cichla monoculus, was more commonly infected by the introduced trematode parasite Centrocestus formosanus than were three other common cichlid fishes. Laboratory infection experiments were conducted to determine whether parasitism might be driven by differential encounter/exposure to parasites or by differential infection susceptibility/preference across different host species. These experiments were performed by controlling for parasite exposure in single host (compatibility) experiments and in mixed host (preference) experiments. In all cases, the peacock bass exhibited higher infection rates with viable metacercariae relative to the other potential fish hosts. Our experiments thus support that an introduced generalist parasite shows apparent specialisation on a specific novel host. Further studies are needed to determine whether these patterns of specialisation are the result of local adaptation following invasion by the parasite.

Testing for local host-parasite adaptation: an experiment with Gyrodactylus ectoparasites and guppy hosts.

Hosts and parasites are in a perpetual co-evolutionary "arms race". Due to their short generation time and large reproductive output, parasites are commonly believed to be ahead in this race, although increasing evidence exists that parasites are not always ahead in the arms race - in part owing to evolutionary lineage and recent ecological history. We assess local adaptation of hosts and parasites, and determine whether adaptation was influenced by ecological or evolutionary history, using full reciprocal cross-infections of four Gyrodactylus ectoparasite populations and their four guppy (Poecilia reticulata) host populations in Trinidad. To consider effects of evolutionary lineage and recent ecology, these four populations were collected from two different river drainages (Marianne and Aripo) and two different predation environments (high and low). The highest infection levels were obtained when parasites from the Aripo lineage infected guppies from the Marianne lineage, indicating a higher infectivity, virulence and/or reproductive success of the Aripo parasites. Aripo lineage guppies were also better able to limit Gyrodactylus population growth than guppies from the Marianne River, indicating their strong "resistance" to Gyrodactylus regardless of the source of the parasite. Predation environment had no detectable influence on host-parasite population dynamics of sympatric or allopatric combinations. The much stronger effect of evolutionary lineage (i.e., river) than recent ecological history (i.e., predation) emphasises its importance in driving co-evolutionary dynamics, and should be explored further in future studies on local host-parasite adaptation.

Two decades of genetic profiling yields first evidence of natal philopatry and long-term fidelity to parturition sites in sharks.

Sharks are a globally threatened group of marine fishes that often breed in their natal region of origin. There has even been speculation that female sharks return to their exact birthplace to breed ('natal philopatry'), which would have important conservation implications. Genetic profiling of lemon sharks (Negaprion brevirostris) from 20 consecutive cohorts (1993-2012) at Bimini, Bahamas, showed that certain females faithfully gave birth at this site for nearly two decades. At least six females born in the 1993-1997 cohorts returned to give birth 14-17 years later, providing the first direct evidence of natal philopatry in the chondrichthyans. Long-term fidelity to specific nursery sites coupled with natal philopatry highlights the merits of emerging spatial and local conservation efforts for these threatened predators.

Exploring possible human influences on the evolution of Darwin's finches.

Humans are an increasingly common influence on the evolution of natural populations. Potential arenas of influence include altered evolutionary trajectories within populations and modifications of the process of divergence among populations. We consider this second arena in the medium ground finch (Geospiza fortis) on Santa Cruz Island, Galápagos, Ecuador. Our study compared the G. fortis population at a relatively undisturbed site, El Garrapatero, to the population at a severely disturbed site, Academy Bay, which is immediately adjacent to the town of Puerto Ayora. The El Garrapatero population currently shows beak size bimodality that is tied to assortative mating and disruptive selection, whereas the Academy Bay population was historically bimodal but has lost this property in conjunction with a dramatic increase in local human population density. We here evaluate potential ecological-adaptive drivers of the differences in modality by quantifying relationships between morphology (beak and head dimensions), functional performance (bite force), and environmental characteristics (diet). Our main finding is that associations among these variables are generally weaker at Academy Bay than at El Garrapatero, possibly because novel foods are used at the former site irrespective of individual morphology and performance. These results are consistent with the hypothesis that the rugged adaptive landscapes promoting and maintaining diversification in nature can be smoothed by human activities, thus hindering ongoing adaptive radiation.

Both geography and ecology contribute to mating isolation in guppies.

Local adaptation to different environments can promote mating isolation--either as an incidental by-product of trait divergence, or as a result of selection to avoid maladaptive mating. Numerous recent empirical examples point to the common influence of divergent natural selection on speciation based largely on evidence of strong pre-mating isolation between populations from different habitat types. Accumulating evidence for natural selection's influence on speciation is therefore no longer a challenge. The difficulty, rather, is in determining the mechanisms involved in the progress of adaptive divergence to speciation once barriers to gene flow are already present. Here, we present results of both laboratory and field experiments with Trinidadian guppies (Poecilia reticulata) from different environments, who do not show complete reproductive isolation despite adaptive divergence. We investigate patterns of mating isolation between populations that do and do not exchange migrants and show evidence for both by-product and reinforcement mechanisms depending on female ecology. Specifically, low-predation females discriminate against all high-predation males thus implying a by-product mechanism, whereas high-predation females only discriminate against low-predation males from further upstream in the same river, implying selection to avoid maladaptive mating. Our study thus confirms that mechanisms of adaptive speciation are not necessarily mutually exclusive and uncovers the complex ecology-geography interactions that underlie the evolution of mating isolation in nature.

Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin's finches.

Divergence and speciation can sometimes proceed in the face of, and even be enhanced by, ongoing gene flow. We here study divergence with gene flow in Darwin's finches, focusing on the role of ecological/adaptive differences in maintaining/promoting divergence and reproductive isolation. To this end, we survey allelic variation at 10 microsatellite loci for 989 medium ground finches (Geospiza fortis) on Santa Cruz Island, Galápagos. We find only small genetic differences among G. fortis from different sites. We instead find noteworthy genetic differences associated with beak. Moreover, G. fortis at the site with the greatest divergence in beak size also showed the greatest divergence at neutral markers; i.e. the lowest gene flow. Finally, morphological and genetic differentiation between the G. fortis beak-size morphs was intermediate to that between G. fortis and its smaller (Geospiza fuliginosa) and larger (Geospiza magnirostris) congeners. We conclude that ecological differences associated with beak size (i.e. foraging) influence patterns of gene flow within G. fortis on a single island, providing additional support for ecological speciation in the face of gene flow. Patterns of genetic similarity within and between species also suggest that interspecific hybridization might contribute to the formation of beak-size morphs within G. fortis.

Spatiotemporal variation in linear natural selection on body color in wild guppies (Poecilia reticulata).

We conducted 10 mark-recapture experiments in natural populations of Trinidadian guppies to test hypotheses concerning the role of viability selection in geographic patterns of male color variation. Previous work has reported that male guppies are more colorful in low-predation sites than in high-predation sites. This pattern of phenotypic variation has been theorized to reflect differences in the balance between natural (viability) selection that disfavors bright male color (owing to predation) and sexual selection that favors bright color (owing to female choice). Our results support the prediction that male color is disfavored by viability selection in both predation regimes. However, it does not support the prediction that viability selection against male color is weaker in low-predation experiments. Instead, some of the most intense bouts of selection against color occurred in low-predation experiments. Our results illustrate considerable spatiotemporal variation in selection among experiments, but such variation was not generally correlated with local patterns of color diversity. More complex selective interactions, possibly including the indirect effects of predators on variation in mating behavior, as well as other environmental factors, might be required to more fully explain patterns of secondary sexual trait variation in this system.

Adaptive changes in life history and survival following a new guppy introduction.

Numerous studies of wild populations have shown that phenotypic traits can change adaptively on short timescales, but very few studies have considered coincident changes in major fitness components. We here examine adaptive changes in life-history traits and survival rates for wild guppies introduced into new environments. Female life-history traits in the derived (Damier River) populations diverged from the ancestral (Yarra River) population, as a result of adaptation to predation regime (high vs. low) and other aspects of the local river. Moreover, some components of the derived Damier populations, particularly juveniles, now show higher survival in the Damier than do contemporary representatives from the ancestral Yarra population. These results suggest that adaptive change can improve survival rates after fewer than 10 years (fewer than 30 guppy generations) in a new environment.

Evolutionary potential of a large marine vertebrate: quantitative genetic parameters in a wild population.

Estimating quantitative genetic parameters ideally takes place in natural populations, but relatively few studies have overcome the inherent logistical difficulties. For this reason, no estimates currently exist for the genetic basis of life-history traits in natural populations of large marine vertebrates. And yet such estimates are likely to be important given the exposure of this taxon to changing selection pressures, and the relevance of life-history traits to population productivity. We report such estimates from a long-term (1995-2007) study of lemon sharks (Negaprion brevirostris) conducted at Bimini, Bahamas. We obtained these estimates by genetically reconstructing a population pedigree (117 dams, 487 sires, and 1351 offspring) and then using an "animal model" approach to estimate quantitative genetic parameters. We find significant additive genetic (co)variance, and hence moderate heritability, for juvenile length and mass. We also find substantial maternal effects for these traits at age-0, but not age-1, confirming that genotype-phenotype interactions between mother and offspring are strongest at birth; although these effects could not be parsed into their genetic and nongenetic components. Our results suggest that human-imposed selection pressures (e.g., size-selective harvesting) might impose noteworthy evolutionary change even in large marine vertebrates. We therefore use our findings to explain how maternal effects may sometimes promote maladaptive juvenile traits, and how lemon sharks at different nursery sites may show "constrained local adaptation." We also show how single-generation pedigrees, and even simple marker-based regression methods, can provide accurate estimates of quantitative genetic parameters in at least some natural systems.

Environmental factors influencing adult sex ratio in Trinidadian guppies.

Sex ratios can influence mating behaviour, population dynamics and evolutionary trajectories; yet the causes of natural sex ratio variation are often uncertain. Although secondary (birth) sex ratios in guppies (Poecilia reticulata) are typically 1:1, we recorded female-biased tertiary (adult) sex ratios in about half of our 48 samples and male-biased sex ratios in none of them. This pattern implies that some populations experience male-biased mortality, perhaps owing to variation in predation or resource limitation. We assessed the effects of predation and/or inter-specific resource competition (intraguild predation) by measuring the local catch-per-unit-effort (CPUE) of species (Rivulus killifish and Macrobrachium prawns) that may differentially prey on male guppies. We assessed the effects of resource levels by measuring canopy openness and algal biomass (chlorophyll a concentration). We found that guppy sex ratios were increasingly female-biased with increasing CPUE of Macrobrachium, and perhaps also Rivulus, and with decreasing canopy openness. We also found an interaction between predators and resource levels in that the effect of canopy openness was greatest when Macrobrachium CPUE was highest. Our study thus also reveals the value of simultaneously testing multiple environmental factors that may drive tertiary sex ratio variation.

Disruptive selection in a bimodal population of Darwin's finches.

A key part of the ecological theory of adaptive radiation is disruptive selection during periods of sympatry. Some insight into this process might be gained by studying populations that are bimodal for dual-context traits, i.e. those showing adaptive divergence and also contributing to reproductive isolation. A population meeting these criteria is the medium ground finch (Geospiza fortis) of El Garrapatero, Santa Cruz Island, Galápagos. We examined patterns of selection in this population by relating individual beak sizes to interannual recaptures during a prolonged drought. Supporting the theory, disruptive selection was strong between the two beak size modes. We also found some evidence of selection against individuals with the largest and smallest beak sizes, perhaps owing to competition with other species or to gaps in the underlying resource distribution. Selection may thus simultaneously maintain the current bimodality while also constraining further divergence. Spatial and temporal variation in G. fortis bimodality suggests a dynamic tug of war among factors such as selection and assortative mating, which may alternatively promote or constrain divergence during adaptive radiation.

Reproductive isolation of sympatric morphs in a population of Darwin's finches.

Recent research on speciation has identified a central role for ecological divergence, which can initiate speciation when (i) subsets of a species or population evolve to specialize on different ecological resources and (ii) the resulting phenotypic modes become reproductively isolated. Empirical evidence for these two processes working in conjunction, particularly during the early stages of divergence, has been limited. We recently described a population of the medium ground finch, Geospiza fortis, that features large and small beak morphs with relatively few intermediates. As in other Darwin's finches of the Galápagos Islands, these morphs presumably diverged in response to variation in local food availability and inter- or intraspecific competition. We here demonstrate that the two morphs show strong positive assortative pairing, a pattern that holds over three breeding seasons and during both dry and wet conditions. We also document restrictions on gene flow between the morphs, as revealed by genetic variation at 10 microsatellite loci. Our results provide strong support for the central role of ecology during the early stages of adaptive radiation.

The relative influence of natural selection and geography on gene flow in guppies.

Two general processes may influence gene flow among populations. One involves divergent selection, wherein the maladaptation of immigrants and hybrids impedes gene flow between ecological environments (i.e. ecological speciation). The other involves geographic features that limit dispersal. We determined the relative influence of these two processes in natural populations of Trinidadian guppies (Poecilia reticulata). If selection is important, gene flow should be reduced between different selective environments. If geography is important, gene flow should be impeded by geographic distance and physical barriers. We examined how genetic divergence, long-term gene flow, and contemporary dispersal within a watershed were influenced by waterfalls, geographic distance, predation, and habitat features. We found that waterfalls and geographic distance increased genetic divergence and reduced dispersal and long-term gene flow. Differences in predation or habitat features did not influence genetic divergence or gene flow. In contrast, differences in predation did appear to reduce contemporary dispersal. We suggest that the standard predictions of ecological speciation may be heavily nuanced by the mating behaviour and life history strategies of guppies.