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Evolutionary history of the endangered fish Zoogoneticus quitzeoensis (Bean, 1898) (Cyprinodontiformes: Goodeidae) using a sequential approach to phylogeography based on mitochondrial and nuclear DNA data.

ABSTRACT: BACKGROUND:Tectonic, volcanic and climatic events that produce changes in hydrographic systems are the main causes of diversification and speciation of freshwater fishes. Elucidate the evolutionary history of freshwater fishes permits to infer theories on the biotic and geological evolution of a region, which can further be applied to understand processes of population divergence, speciation and for conservation purposes. The freshwater ecosystems in Central Mexico are characterized by their genesis dynamism, destruction, and compartmentalization induced by intense geologic activity and climatic changes since the early Miocene. The endangered goodeid Zoogoneticus quitzeoensis is widely distributed across Central México, thus making it a good model for phylogeographic analyses in this area. RESULTS:We addressed the phylogeography, evolutionary history and genetic structure of populations of Z. quitzeoensis through a sequential approach, based on both microsatellite and mitochondrial cytochrome b sequences. Most haplotypes were private to particular locations. All the populations analysed showed a remarkable number of haplotypes. The level of gene diversity within populations was Hd = 0.987 (0.714 - 1.00). However, in general the nucleotide diversity was low, pi = 0.0173 (0.0015 - 0.0049). Significant genetic structure was found among populations at the mitochondrial and nuclear level (PhiST = 0.836 and FST = 0.262, respectively). We distinguished two well-defined mitochondrial lineages that were separated ca. 3.3 million years ago (Mya). The time since expansion was ca. 1.5 x 10(6) years ago for Lineage I and ca. 860,000 years ago for Lineage II. Also, genetic patterns of differentiation, between and within lineages, are described at different historical timescales. CONCLUSION:Our mtDNA data indicates that the evolution of the different genetic groups is more related to ancient geological and climatic events (Middle Pliocene, ca. 3.3 Mya) than to the current hydrographic configuration of the basins. In general, mitochondrial and nuclear data supported the same relationships between populations, with the exception of some reduced populations in highly polluted basins (Lower Lerma River), where the effects of genetic drift are suggested by the different analyses at the nuclear and mitochondrial level. Further, our findings are of special interest for the conservation of this endangered species.

SUBMITTER: Dominguez-Dominguez O

PROVIDER: S-EPMC2435552 | biostudies-literature | 2008 May

REPOSITORIES: biostudies-literature

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Evolutionary history of the endangered fish Zoogoneticus quitzeoensis (Bean, 1898) (Cyprinodontiformes: Goodeidae) using a sequential approach to phylogeography based on mitochondrial and nuclear DNA data.

Domínguez-Domínguez Omar O Alda Fernando F de León Gerardo Pérez-Ponce GP García-Garitagoitia José Luis JL Doadrio Ignacio I

BMC evolutionary biology 20080526

<h4>Background</h4>Tectonic, volcanic and climatic events that produce changes in hydrographic systems are the main causes of diversification and speciation of freshwater fishes. Elucidate the evolutionary history of freshwater fishes permits to infer theories on the biotic and geological evolution of a region, which can further be applied to understand processes of population divergence, speciation and for conservation purposes. The freshwater ecosystems in Central Mexico are characterized by t ...[more]

PMID: 18503717

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Project description:BACKGROUND:One of the most perplexing questions in evolutionary biology is why some lineages diversify into many species, and others do not. In many cases, ecological opportunity has played an important role, leading to diversification along trophic or habitat-based axes. The Goodeidae (Teleostomi: Cyprinodontiformes) are a family of freshwater fishes with two subfamilies: Goodeinae (42 species, viviparous, heterogeneous habitats, Mesa Central of Mexico) and Empetrichthyinae (4 species, oviparous, homogeneous habitats, Great Basin of the United States). These discrepant sets of characteristics and their sister-group relationship make the goodeids amenable to a comparative study of diversification. We gathered lateral body images from more than 1600 specimens of all extant species in the family. Geometric morphometric, and phylogenetic comparative analyses were used to address whether higher species diversity correlates with higher rates of morphological shape evolution and whether there are differences in functional/habitat modules between the two subfamilies. RESULTS:This study recovered a higher rate of overall body shape evolution in the Goodeinae that is nearly double in magnitude compared to the Empetrichthyinae. A modularity test indicated that the Goodeinae displayed elevated rates of morphological evolution in comparison to the Empetrichthyinae when only trunk (locomotor) regions were compared between subfamilies. No significant differences in evolutionary shape rates were recovered when the trophic (head) regions were compared between subfamilies. DISCUSSION:These results support the hypothesis that Mexican goodeids radiated via an ecological opportunity scenario into a wide-array of novel habitats in the island-like Mesa Central as evidenced by their high rate of shape evolution, relative to the Empetrichthyinae. This study quantitatively unraveled the drivers of evolution and eliminated trophic specialization as a driving force within the Goodeidae. CONCLUSIONS:A combination of phylogenetic and morphometric data, and phylogenetic comparative analyses were used to examine body shape rate evolution within the Goodeidae. Results support the hypothesis that species in the subfamily Goodeinae on the central Mexican plateau had a higher rate of body shape evolution relative to its sister subfamily Empetrichthyinae in the Great Basin suggesting that the Goodeinae diversified via an ecological opportunity scenario along habitat, rather than trophic axes.

Project description:North America's Great Basin has long been of interest to biologists due to its high level of organismal endemicity throughout its endorheic watersheds. One example of such a group is the subfamily Empetricthyinae. In this paper, we analyzed the relationships of the Empetrichtyinae and assessed the validity of the subspecies designations given by Williams and Wilde within the group using concatenated phylogenetic tree estimation and species tree estimation. Samples from 19 populations were included covering the entire distribution of the three extant species of Empetricthyinae-Crenichthys nevadae, Crenichthys baileyi and Empetricthys latos. Three nuclear introns (S8 intron 4, S7 intron 1, and P0 intron 1) and one mitochondrial gene (Cytb) were sequenced for phylogenetic analysis. Using these sequences, we generated two separate hypotheses of the evolutionary relationships of Empetrichtyinae- one based on the mitochondrial data and one based on the nuclear data using Bayesian phylogenetics. Haplotype networks were also generated to look at the relationships of the populations within Empetrichthyinae. After comparing the two phylogenetic hypotheses, species trees were generated using *BEAST with the nuclear data to further test the validity of the subspecies within Empetrichthyinae. The mitochondrial analyses supported four lineages within C. baileyi and 2 within C. nevadae. The concatenated nuclear tree was more conserved, supporting one clade and an unresolved polytomy in both species. The species tree analysis supported the presence of two species within both C. baileyi and C. nevadae. Based on the results of these analyses, the subspecies designations of Williams and Wilde are not valid, rather a conservative approach suggests there are two species within C. nevadae and two species within C. baileyi. No structure was found for E. latos or the populations of Empetricthyinae. This study represents one of many demonstrating the invalidity of subspecies and their detriment to species identification, conservation, and understanding.

Project description:A central goal of comparative phylogeography is determining whether codistributed species experienced (1) concerted evolutionary responses to past geological and climatic events, indicated by congruent spatial and temporal patterns ("concerted-response hypothesis"); (2) independent responses, indicated by spatial incongruence ("independent-response hypothesis"); or (3) multiple responses ("multiple-response hypothesis"), indicated by spatial congruence but temporal incongruence ("pseudocongruence") or spatial and temporal incongruence ("pseudoincongruence"). We tested these competing hypotheses using DNA sequence data from three livebearing fish species codistributed in the Nicaraguan depression of Central America (Alfaro cultratus, Poecilia gillii, and Xenophallus umbratilis) that we predicted might display congruent responses due to co-occurrence in identical freshwater drainages. Spatial analyses recovered different subdivisions of genetic structure for each species, despite shared finer-scale breaks in northwestern Costa Rica (also supported by phylogenetic results). Isolation-with-migration models estimated incongruent timelines of among-region divergences, with A. cultratus and Xenophallus populations diverging over Miocene-mid-Pleistocene while P. gillii populations diverged over mid-late Pleistocene. Approximate Bayesian computation also lent substantial support to multiple discrete divergences over a model of simultaneous divergence across shared spatial breaks (e.g., Bayes factor [B 10] = 4.303 for Ψ [no. of divergences] > 1 vs. Ψ = 1). Thus, the data support phylogeographic pseudoincongruence consistent with the multiple-response hypothesis. Model comparisons also indicated incongruence in historical demography, for example, support for intraspecific late Pleistocene population growth was unique to P. gillii, despite evidence for finer-scale population expansions in the other taxa. Empirical tests for phylogeographic congruence indicate that multiple evolutionary responses to historical events have shaped the population structure of freshwater species codistributed within the complex landscapes in/around the Nicaraguan depression. Recent community assembly through different routes (i.e., different past distributions or colonization routes), and intrinsic ecological differences among species, has likely contributed to the unique phylogeographical patterns displayed by these Neotropical fishes.

Project description:The evolution of the Yunnan Plateau's drainages network during the Pleistocene was dominated by the intense uplifts of the Qinghai-Tibetan Plateau. In the present study, we investigated the association between the evolutionary histories of three main drainage systems and the geographic patterns of genetic differentiation of Poropuntius huangchuchieni.We sequenced the complete sequences of mitochondrial control region for 304 specimens and the sequences of Cytochrome b gene for 15 specimens of the species P. huangchuchieni and 5 specimens of Poropuntius opisthoptera. Phylogenetic analysis identified five major lineages, of which lineages MK-A and MK-B constrained to the Mekong River System, lineages RL and LX to the Red River System, and lineage SW to the Salween River System. The genetic distance and network analysis detected significant divergences among these lineages. Mismatch distribution analysis implied that the population of P. huangchuchieni underwent demographic stability and the lineage MK-B, sublineages MK-A1 and LX-1 underwent a recent population expansion. The divergence of the 5 major lineages was dated back to 0.73-1.57 MYA.Our results suggest that P. opisthoptera was a paraphyletic group of P. huangchuchieni. The phylogenetic pattern of P. huangchuchieni was mostly associated with the drainage's structures and the geomorphological history of the Southwest Yunnan Plateau. Also the differentiation of the major lineages among the three drainages systems coincides with the Kunlun-Yellow River Movement (1.10-0.60 MYA). The genetic differentiation within river basins and recent demographical expansions that occurred in some lineages and sublineages are consistent with the palaeoclimatic oscillations during the Pleistocene. Additionally, our results also suggest that the populations of P. huangchuchieni had keep long term large effective population sizes and demographic stability in the recent evolutionary history, which may be responsible for the high genetic diversity and incomplete lineages sorting of Poropuntius huangchuchieni.

Dataset Information

Evolutionary history of the endangered fish Zoogoneticus quitzeoensis (Bean, 1898) (Cyprinodontiformes: Goodeidae) using a sequential approach to phylogeography based on mitochondrial and nuclear DNA data.

Publications

Evolutionary history of the endangered fish Zoogoneticus quitzeoensis (Bean, 1898) (Cyprinodontiformes: Goodeidae) using a sequential approach to phylogeography based on mitochondrial and nuclear DNA data.

Similar Datasets

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