Morphologic and genetic variation within a relict Andean catfish, Hatcheria macraei , and its relationship with Trichomycterus areolatus and Bullockia maldonadoi (Siluriformes: Trichomycteridae).

The South American siluriform fishes are found primarily in the Neotropical region, north and east of the Colorado River of Argentina, with a few relict species distributed southward and westward on both sides of the Andes Mountains. Three of these, the closely related trichomycterids Hatcheria macraei, Trichomycterus areolatus and Bullockia maldonadoi, have been subject to historical taxonomic and nomenclatural arrangements. Here, we amplify a 652-bp fragment of COI mtDNA from 55 H. macraei individuals and use publicly available Cytb mtDNA sequences of the three taxa to assess their relationship, genetic variation and haplotype distribution in relation to hydrographic basins. In addition, we extend a recent morphometric study on H. macraei by analyzing body shape in 447 individuals collected from 24 populations across their entire cis-Andean distribution. We identified some lineages previously assigned to T. areolatus that show a closer relationship to either B. maldonadoi or H. macraei, revealing new boundaries to their currently known trans-Andean distribution. We found a great morphologic variation among H. macraei populations and a high genetic variation in H. macraei, T. areolatus and B. maldonadoi associated with river basins. We highlight further integrative studies are needed to enhance our knowledge of the southern Andean trichomycterid diversity.

Beyond Pairwise Interactions: Multispecies Character Displacement in Mexican Freshwater Fish Communities.

Competition has long been recognized as a central force in shaping evolution, particularly through character displacement. Yet research on character displacement is biased, as it has focused almost exclusively on pairs of interacting species while ignoring multispecies interactions. Communities are seldom so simple that only pairs of species interact, and it is not clear whether inferences from pairwise interactions are sufficient to explain patterns of phenotypes in nature. Here, we test for character displacement in a natural system of freshwater fishes in western Mexico that contains up to four congeneric species of the genus Poeciliopsis. We analyzed body shape differences between populations with different numbers of competitors while accounting for confounding environmental variables. Surprisingly, we found evidence for convergent character displacement in populations of P. prolifica, P. viriosa, and P. latidens. We also found that the convergence in body shape was not consistently in the same direction, meaning that when three or more competitors co-occurred, we did not find more extreme body shapes compared with when there were only two competitors. Instead, when three or more competitors co-occurred, body shape was intermediate between the shape found with a pair of species and the shape found with no competitor present. This intermediate shape suggests that evolution in multispecies communities likely occurs in response to several competitors rather than to simple pairwise interactions. Overall, our results suggest that competition among multiple species is more complex than simple pairwise competitive interactions.

Divergent predation environment between two sister species of livebearing fishes (Cyprinodontiformes: Poeciliidae) predicts boldness, activity, and exploration behavior / Ambientes de depredación divergente para dos especies hermanas de peces vivíparos (Cyprinodontiformes: Poeciliidae) predicen el comportamiento de audacia, actividad y exploración

Abstract:Predators can influence a variety of prey traits, including behavior. Traits such as boldness, activity rate, and tendency to explore can all be shaped by predation risk. Our study examines the effects of predation on these behaviors by considering a natural system in which two sister species of livebearing fishes, Brachyrhaphis roseni and B. terrabensis, experience divergent predation environments. In February of 2013, we collected fish in the Río Chiriquí Nuevo drainage, Chiriquí, Panama, and conducted behavioral assays. Using open-field behavioral assays, we evaluated both juveniles and adults, and males and females, to determine if there were differences in behavior between ontogenetic stages or between sexes. We assessed boldness as 'time to emerge' from a shelter into a novel environment, and subsequently measured activity and exploration within that novel environment. We predicted that B. roseni (a species that co-occurs with predators) would be more bold, more active, and more prone to explore, than B. terrabensis (a species that does not co-occur with predators). In total, we tested 17 juveniles, 21 adult males, and 20 adult females of B. roseni, and 19 juveniles, 19 adult males, and 18 adult females of B. terrabensis. We collected all animals from streams in Chiriquí, Panama in February 2013, and tested them following a short acclimation period to laboratory conditions. As predicted, we found that predation environment was associated with several differences in behavior. Both adult and juvenile B. roseni were more active and more prone to explore than B. terrabensis. However, we found no differences in boldness in either adults or juveniles. We also found a significant interaction between 'sex' and 'species' as predictors of boldness and exploration, indicating that predation environment can affect behaviors of males and females differently in each species. Our work demonstrates the importance of considering sex and life history stage when evaluating the evolution of behavior. Rev. Biol. Trop. 65 (1): 267-277. Epub 2017 March 01.

ResumenLos depredadores pueden influenciar una variedad de rasgos de la presa, incluyendo el comportamiento. Los rasgos tales como la audacia, nivel de actividad, y la tendencia a explorar; pueden ser moldeados por el riesgo de depredación. Nuestro estudio examina los efectos de la depredación en el comportamiento al considerar un sistema natural en el que dos especies hermanas de peces vivíparos, Brachyrhaphis roseni y B. terrabensis, se presentan en ambientes de depredación divergente. En febrero 2013, recolectamos peces en el drenaje del Río Chiriquí Nuevo, Chiriquí, Panamá y llevamos a cabo ensayos de comportamiento. Al usar ensayos de comportamiento en campo abierto, se evaluó el comportamiento en juveniles y adultos, machos y hembras, para determinar si los patrones de divergencia diferían entre las etapas ontogenéticas o entre sexos. Se evaluó la audacia como "tiempo en salir" de un refugio a un ambiente nuevo, y posteriormente se midió la actividad y la exploración dentro de ese nuevo ambiente. Nosotros predijimos que B. roseni (una especie que se presenta con los depredadores) sería más audaz, activa y propensa a explorar que B. terrabensis (una especie que no se presenta con los depredadores). En total, probamos 17 jóvenes, 21 machos adultos, y 20 hembras adultas de B. roseni, y 19 jóvenes, 19 machos adultos, y 18 hembras adultas de B. terrabensis. Recogimos todos los animales en Chiriquí, Panamá en Febrero 2013, y los probamos después de un corto período de aclimatación a las condiciones de laboratorio. Como se predijo, se encontró que la depredación ambiental se asoció con varias diferencias en el comportamiento. Tanto adultos y jóvenes de B. roseni eran más activos y más propensos a explorar que B. terrabensis. Sin embargo, no se encontraron diferencias en la audacia en adultos o menores. También se encontró una interacción significativa entre "sexo" y "especie" como predictores de la audacia y la exploración, lo que indica que la depredación puede afectar el comportamiento de los machos y hembras de manera diferente en cada especie. Nuestro estudio demuestra la importancia de considerar el sexo y la etapa del ciclo de vida al evaluar la evolución del comportamiento.

Divergent predation environment between two sister species of livebearing fishes (Cyprinodontiformes: Poeciliidae) predicts boldness, activity, and exploration behavior.

Predators can influence a variety of prey traits, including behavior. Traits such as boldness, activity rate, and tendency to explore can all be shaped by predation risk. Our study examines the effects of predation on these behaviors by considering a natural system in which two sister species of livebearing fishes, Brachyrhaphis roseni and B. terrabensis, experience divergent predation environments. In February of 2013, we collected fish in the Río Chiriquí Nuevo drainage, Chiriquí, Panama, and conducted behavioral assays. Using open-field behavioral assays, we evaluated both juveniles and adults, and males and females, to determine if there were differences in behavior between ontogenetic stages or between sexes. We assessed boldness as 'time to emerge' from a shelter into a novel environment, and subsequently measured activity and exploration within that novel environment. We predicted that B. roseni (a species that co-occurs with predators) would be more bold, more active, and more prone to explore, than B. terrabensis (a species that does not co-occur with predators). In total, we tested 17 juveniles, 21 adult males, and 20 adult females of B. roseni, and 19 juveniles, 19 adult males, and 18 adult females of B. terrabensis. We collected all animals from streams in Chiriquí, Panama in February 2013, and tested them following a short acclimation period to laboratory conditions. As predicted, we found that predation environment was associated with several differences in behavior. Both adult and juvenile B. roseni were more active and more prone to explore than B. terrabensis. However, we found no differences in boldness in either adults or juveniles. We also found a significant interaction between 'sex' and 'species' as predictors of boldness and exploration, indicating that predation environment can affect behaviors of males and females differently in each species. Our work demonstrates the importance of considering sex and life history stage when evaluating the evolution of behavior.

Low Genetic Diversity in Diplomystes camposensis, an Endemic and Endangered Catfish from South Chile.

Carlos P. Muñoz-Ramírez, Evelyn Habit, Peter J. Unmack, Jerald B. Johnson, and Pedro F. Victoriano (2016) Despite the fundamental importance of the family Diplomystidae for understanding catfish evolution, its species are poorly known and most of them endangered. Diplomystes camposensis, restricted to a single river basin in southern Chile, is perhaps the most vulnerable species due to its small geographic range and imminent habitat alterations by dam constructions. Using mitochondrial DNA sequences, we describe the genetic diversity across its entire distribution in the Valdivia basin and test hypotheses related to the impact of glacial cycles on the genetic diversity and structure. We found that Diplomystes camposensis has low genetic diversity and structure across the entire Valdivia basin along with a pattern of decreasing nucleotide and haplotype diversity from West to East. Demographic analyses showed evidence of population expansion in agreement with the glaciated history of the basin. Analyses of population structure showed no evidence of population subdivision. However, coalescent analyses indicated that very recent subdivision (in the last 50 years) cannot be ruled out. Low genetic diversity and genetic structure across the entire basin suggest that the species might be highly vulnerable to habitat fragmentation. Thus, the imminent construction of hydropower dams represents a serious threat to its conservation. Our results suggest that the low genetic diversity can be the product of the glaciated history of the basin, although the influence of species-specific biological traits may also add to this condition. Despite the overall low genetic diversity, higher diversity was found in the central portion of the basin suggesting high priority of conservation for this area as it might be used as a source population in case translocations are required among potential management plans.

Phylogenetic analyses provide insights into the historical biogeography and evolution of Brachyrhaphis fishes.

The livebearing fish genus Brachyrhaphis (Poeciliidae) has become an increasingly important model in evolution and ecology research, yet the phylogeny of this group is not well understood, nor has it been examined thoroughly using modern phylogenetic methods. Here, we present the first comprehensive phylogenetic analysis of Brachyrhaphis by using four molecular markers (3mtDNA, 1nucDNA) to infer relationships among species in this genus. We tested the validity of this genus as a monophyletic group using extensive outgroup sampling based on recent phylogenetic hypotheses of Poeciliidae. We also tested the validity of recently described species of Brachyrhaphis that are part of the B. episcopi complex in Panama. Finally, we examined the impact of historical events on diversification of Brachyrhaphis, and made predictions regarding the role of different ecological environments on evolutionary diversification where known historical events apparently fail to explain speciation. Based on our results, we reject the monophyly of Brachyrhaphis, and question the validity of two recently described species (B. hessfeldi and B. roswithae). Historical biogeography of Brachyrhaphis generally agrees with patterns found in other freshwater taxa in Lower Central America, which show that geological barriers frequently predict speciation. Specifically, we find evidence in support of an 'island' model of Lower Central American formation, which posits that the nascent isthmus was partitioned by several marine connections before linking North and South America. In some cases where historic events (e.g., vicariance) fail to explain allopatric species breaks in Brachyrhaphis, ecological processes (e.g., divergent predation environments) offer additional insight into our understanding of phylogenetic diversification in this group.

Phylogeography and biogeography of the lower Central American Neotropics: diversification between two continents and between two seas.

Lower Central America (LCA) provides a geologically complex and dynamic, richly biodiverse model for studying the recent assembly and diversification of a Neotropical biota. Here, we review the growing literature of LCA phylogeography studies and their contribution to understanding the origins, assembly, and diversification of the LCA biota against the backdrop of regional geologic and climatic history, and previous biogeographical inquiry. Studies to date reveal that phylogeographical signal within taxa of differing distributions reflects a diversity of patterns and processes rivalling the complexities of LCA landscapes themselves. Even so, phylogeography is providing novel insights into regional diversification (e.g. cryptic lineage divergences), and general evolutionary patterns are emerging. Congruent multi-taxon phylogeographic breaks are found across the Nicaraguan depression, Chorotega volcanic front, western and central Panama, and the Darién isthmus, indicating that a potentially shared history of responses to regional-scale (e.g. geological) processes has shaped the genetic diversity of LCA communities. By contrast, other species show unique demographic histories in response to overriding historical events, including no phylogeographic structure at all. These low-structure or incongruent patterns provide some evidence for a role of local, ecological factors (e.g. long-distance dispersal and gene flow in plants and bats) in shaping LCA communities. Temporally, comparative phylogeographical structuring reflects Pliocene-Pleistocene dispersal and vicariance events consistent with the timeline of emergence of the LCA isthmus and its major physiographic features, e.g. cordilleras. We emphasise the need to improve biogeographic inferences in LCA through in-depth comparative phylogeography projects capitalising on the latest statistical phylogeographical methods. While meeting the challenges of reconstructing the biogeographical history of this complex region, phylogeographers should also take up the critical service to society of applying their work to the conservation of its fascinating biodiversity.

Phylogeography of the catfish Hatcheria macraei reveals a negligible role of drainage divides in structuring populations.

Southern South America provides a set of unusual geographic features that make it particularly interesting for studying phylogeography. The Andes Mountains run along a north-to-south axis and act as a barrier to gene flow for much of the biota of this region, with southern portions experiencing extensive historical glaciation. Geological data reveal a series of drainage reversals, shifting from Pacific Ocean outlets to Atlantic Ocean outlets because of glacier formation that dammed and reversed rivers. Once glaciers melted around 13 000 years ago, drainages returned to the Pacific Ocean. This geologic history predicts that aquatic organisms in Pacific rivers should have their closest relationships to their counterparts in Atlantic rivers immediately to their east. We tested this prediction in the trichomycterid catfish Hatcheria macraei from 38 locations using the mitochondrial cytochrome b gene. Our results show that most populations found in Pacific rivers were closely related to fish found in the adjacent Atlantic draining Río Chubut. Surprisingly, one documented drainage reversal (from Río Deseado into Río Baker) did not result in movement of H. macraei. Overall, we found the lowest levels of genetic structure between most Pacific rivers that are adjacent to the Atlantic draining Río Chubut. We also found low levels of population structuring among three of four contemporary river basins that drain to the Atlantic Ocean. Our findings suggest that drainage basin boundaries have historically not played an important long-term role in structuring between nine of 11 drainages, an unusual finding in freshwater biogeography.

Different processes lead to similar patterns: a test of codivergence and the role of sea level and climate changes in shaping a southern temperate freshwater assemblage.

BACKGROUND: Understanding how freshwater assemblages have been formed and maintained is a fundamental goal in evolutionary and ecological disciplines. Here we use a historical approach to test the hypothesis of codivergence in three clades of the Chilean freshwater species assemblage. Molecular studies of freshwater crabs (Aegla: Aeglidae: Anomura) and catfish (Trichomycterus arealatus: Trichomycteridae: Teleostei) exhibited similar levels of genetic divergences of mitochondrial lineages between species of crabs and phylogroups of the catfish, suggesting a shared evolutionary history among the three clades in this species assemblage. RESULTS: A phylogeny was constructed for Trichomycterus areolatus under the following best-fit molecular models of evolution GTR + I + R, HKY + I, and HKY for cytochrome b, growth hormone, and rag 1 respectively. A GTR + I + R model provided the best fit for both 28S and mitochondrial loci and was used to construct both Aegla phylogenies. Three different diversification models were observed and the three groups arose during different time periods, from 2.25 to 5.05 million years ago (Ma). Cladogenesis within Trichomycterus areolatus was initiated roughly 2.25 Ma (Late Pliocene-Early Pleistocene) some 1.7-2.8 million years after the basal divergences observed in both Aegla clades. These results reject the hypothesis of codivergence. CONCLUSIONS: The similar genetic distances between terminal sister-lineages observed in these select taxa from the freshwater Chilean species assemblage were formed by different processes occurring over the last ~5.0 Ma. Dramatic changes in historic sea levels documented in the region appear to have independently shaped the evolutionary history of each group. Our study illustrates the important role that history plays in shaping a species assemblage and argues against assuming similar patterns equal a shared evolutionary history.

Biogeography of the livebearing fish Poecilia gillii in Costa Rica: are phylogeographical breaks congruent with fish community boundaries?

One of the original goals of phylogeography was to use genetic data to identify historical events that might contribute to breaks among communities. In this study, we examine the phylogeography of a common livebearing fish (Poecilia gillii) from Costa Rica. Our goal was to determine if phylogeographical breaks in this species were congruent with previously defined boundaries among four fish community provinces. We hypothesized that if abiotic factors influence both community boundaries and genetic structuring in P. gillii then we might find four clades within our focal species that were geographically separated along community boundary lines. Similarly, we expected to find most of the genetic variation in P. gillii partitioned among these four geographical regions. We generated DNA sequence data (mitochondrial cytochrome b and nuclear S7 small ribosomal subunit) for 260 individuals from 42 populations distributed across Costa Rica. We analysed these data using phylogenetic (parsimony and likelihood) and coalescent approaches to estimate phylogenetic relationships among haplotypes, patterns of gene flow and effective population size. Contrary to our expectations, we did not find four monophyletic groups that mapped cleanly to our geographical community provinces. However, one of our clades was restricted to a single province, suggesting that common earth history events could be responsible for both genetic structuring in P. gillii and fish community composition in this area. However, our results show a complex pattern of gene flow throughout other regions in Costa Rica where genetic structuring is not predicted by community province boundaries.

Phylogeography of the livebearer Xenophallus umbratilis (Teleostei: Poeciliidae): glacial cycles and sea level change predict diversification of a freshwater tropical fish.

The biogeography of Central America is viewed as a classic case study in understanding the impact of vicariant events on patterns of biotic dispersal. While many biogeographers have focused on community composition and geographical limits of species at broad scales across Central America, much less work has focused on post-colonization diversification patterns at finer scales. The livebearing freshwater fish Xenophallus umbratilis presents an ideal system for determining the impact of recent Earth history events on biodiversity in northern Costa Rica. Here, we test the hypotheses that marine inundation of the San Carlos and northern Limón basins during the Pliocene and Pleistocene has caused genetic fragmentation among X. umbratilis populations, despite contemporary freshwater connections. To test this idea, we collected mitochondrial (cytochrome b) sequence data in 162 individuals taken from 27 localities across northern Costa Rica. We employed a variety of analytical approaches, including: maximum parsimony and maximum likelihood, analysis of molecular variance, and demographic analysis of population size through time. We found four major clades within X. umbratilis, each geographically isolated with no shared haplotypes across drainages. Oddly, clades that occupy adjacent drainages are not always sister taxa in the phylogeny, suggesting that colonization in this species is more complex than a simple model of isolation by distance. All our results are consistent with the hypothesis that changes in sea level associated with glacial eustatic cycles have had an important effect in shaping diversification patterns in this species.