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Taxonomic Uncertainty and the Anomaly Zone: Phylogenomics Disentangle a Rapid Radiation to Resolve Contentious Species (Gila robusta Complex) in the Colorado River.

ABSTRACT: Species are indisputable units for biodiversity conservation, yet their delimitation is fraught with both conceptual and methodological difficulties. A classic example is the taxonomic controversy surrounding the Gila robusta complex in the lower Colorado River of southwestern North America. Nominal species designations were originally defined according to weakly diagnostic morphological differences, but these conflicted with subsequent genetic analyses. Given this ambiguity, the complex was re-defined as a single polytypic unit, with the proposed "threatened" status under the U.S. Endangered Species Act of two elements being withdrawn. Here we re-evaluated the status of the complex by utilizing dense spatial and genomic sampling (n = 387 and >22 k loci), coupled with SNP-based coalescent and polymorphism-aware phylogenetic models. In doing so, we found that all three species were indeed supported as evolutionarily independent lineages, despite widespread phylogenetic discordance. To juxtapose this discrepancy with previous studies, we first categorized those evolutionary mechanisms driving discordance, then tested (and subsequently rejected) prior hypotheses which argued phylogenetic discord in the complex was driven by the hybrid origin of Gila nigra. The inconsistent patterns of diversity we found within G. robusta were instead associated with rapid Plio-Pleistocene drainage evolution, with subsequent divergence within the "anomaly zone" of tree space producing ambiguities that served to confound prior studies. Our results not only support the resurrection of the three species as distinct entities but also offer an empirical example of how phylogenetic discordance can be categorized within other recalcitrant taxa, particularly when variation is primarily partitioned at the species level.

SUBMITTER: Chafin TK

PROVIDER: S-EPMC8449829 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Cases of polydactyly in natural populations of amphibians have attracted great interest from biologists. At the end of the 1940s, the French biologist Jean Rostand discovered a polymorphic syndrome in some water frog (Anura: Pelophylax) populations that included polydactyly and some severe morphological anomalies (he called it 'anomaly P'). The cause of this anomaly remains unknown for 70 years. In a previous study, we obtained anomaly P in the laboratory in tadpoles of water frogs that developed together with molluscs Planorbarius corneus (Mollusca: Gastropoda) collected in the field. We thus proposed the 'trematode hypothesis', according to which the infectious agent responsible for anomaly P is a trematode species. METHODS:Metacercariae from tadpoles with anomaly P were identified using ITS2 gene sequencing as Strigea robusta (Trematoda: Strigeidae). To verify teratogenic features of the species, cercariae of S. robusta were tested for the possibility to cause anomalies. Identification of cercariae species was made using morphological and molecular methods (sequencing of ITS2 and 28S rRNA). The tadpoles were exposed to parasites at four doses of cercariae (control, low, medium and high) and divided into two groups: "early" (at 25-27 Gosner stages) and "late" (at 29-34 Gosner stages) exposure. RESULTS:A total of 58 (72.5%) tadpoles survived until metamorphosis under the dose-dependent experiment with the trematode S. robusta. Differences in the survival rates were observed between the exposed and unexposed tadpoles both in the group of "early" tadpoles and "late" tadpoles. The exposure of tadpoles to the cercariae of S. robusta induced anomaly P in 82% of surviving tadpoles. The severe forms developed only in "early" stages under all doses of cercariae exposure. Polydactyly predominantly developed in the "late" stages; under a light exposure dose, polydactyly also developed in "early" tadpoles. Laboratory-hatched tadpoles reared together with infected snails had different rates of survival and complexity of deformations associated with the period of coexistence. CONCLUSIONS:The experiments with direct cercariae exposure provide compelling evidence that S. robusta leads to anomaly P in tadpoles of water frogs. The manifestation of anomaly P turned out to be dependent on the stage of development, cercariae dose, and the location of the cysts.

Project description:Reliable estimation of phylogeny is central to avoid inaccuracy in downstream macroevolutionary inferences. However, limitations exist in the implementation of concatenated and summary coalescent approaches, and Bayesian and full coalescent inference methods may not yet be feasible for computation of phylogeny using complicated models and large data sets. Here, we explored methodological (e.g., optimality criteria, character sampling, model selection) and biological (e.g., heterotachy, branch length heterogeneity) sources of systematic error that can result in biased or incorrect parameter estimates when reconstructing phylogeny by using the gadiform fishes as a model clade. Gadiformes include some of the most economically important fishes in the world (e.g., Cods, Hakes, and Rattails). Despite many attempts, a robust higher-level phylogenetic framework was lacking due to limited character and taxonomic sampling, particularly from several species-poor families that have been recalcitrant to phylogenetic placement. We compiled the first phylogenomic data set, including 14,208 loci ($>$2.8 M bp) from 58 species representing all recognized gadiform families, to infer a time-calibrated phylogeny for the group. Data were generated with a gene-capture approach targeting coding DNA sequences from single-copy protein-coding genes. Species-tree and concatenated maximum-likelihood (ML) analyses resolved all family-level relationships within Gadiformes. While there were a few differences between topologies produced by the DNA and the amino acid data sets, most of the historically unresolved relationships among gadiform lineages were consistently well resolved with high support in our analyses regardless of the methodological and biological approaches used. However, at deeper levels, we observed inconsistency in branch support estimates between bootstrap and gene and site coefficient factors (gCF, sCF). Despite numerous short internodes, all relationships received unequivocal bootstrap support while gCF and sCF had very little support, reflecting hidden conflict across loci. Most of the gene-tree and species-tree discordance in our study is a result of short divergence times, and consequent lack of informative characters at deep levels, rather than incomplete lineage sorting. We use this phylogeny to establish a new higher-level classification of Gadiformes as a way of clarifying the evolutionary diversification of the order. We recognize 17 families in five suborders: Bregmacerotoidei, Gadoidei, Ranicipitoidei, Merluccioidei, and Macrouroidei (including two subclades). A time-calibrated analysis using 15 fossil taxa suggests that Gadiformes evolved $\sim $79.5 Ma in the late Cretaceous, but that most extant lineages diverged after the Cretaceous-Paleogene (K-Pg) mass extinction (66 Ma). Our results reiterate the importance of examining phylogenomic analyses for evidence of systematic error that can emerge as a result of unsuitable modeling of biological factors and/or methodological issues, even when data sets are large and yield high support for phylogenetic relationships. [Branch length heterogeneity; Codfishes; commercial fish species; Cretaceous-Paleogene (K-Pg); heterotachy; systematic error; target enrichment.].

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Taxonomic Uncertainty and the Anomaly Zone: Phylogenomics Disentangle a Rapid Radiation to Resolve Contentious Species (Gila robusta Complex) in the Colorado River.

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