Evolutionary History of the Live-Bearing Endemic Allotoca diazi Species Complex (Actinopterygii, Goodeinae): Evidence of Founder Effect Events in the Mexican Pre-Hispanic Period

Abstract

The evolutionary history of Mexican ichthyofauna has been strongly linked to natural events, and the impact of pre-Hispanic cultures is little known. The live-bearing fish species Allotoca diazi, Allotoca meeki and Allotoca catarinae occur in areas of biological, cultural and economic importance in central Mexico: Pátzcuaro basin, Zirahuén basin, and the Cupatitzio River, respectively. The species are closely related genetically and morphologically, and hypotheses have attempted to explain their systematics and biogeography. Mitochondrial DNA and microsatellite markers were used to investigate the evolutionary history of the complex. The species complex shows minimal genetic differentiation. The separation of A. diazi and A. meeki was dated to 400–7000 years ago, explained by geological and climate events. A bottleneck and reduction of genetic diversity in Allotoca diazi was detected, attributed to recent climate fluctuations and anthropogenic activity. The isolation of A. catarinae occurred ~1900 years ago. No geological events are documented in the area during this period, but the date is contemporary with P’urhépecha culture settlements. This founder effect represents the first evidence of fish species translocation by a pre-Hispanic culture of Mexico. The response of the complex to climate fluctuation, geological changes and human activity in the past and the future according to the ecological niches predictions indicates areas of vulnerability and important information for conservation. The new genetic information showed that the Allotoca diazi complex consist of two genetic groups with an incomplete lineage sorting pattern: Pátzcuaro and Zirahuén lakes, and an introduced population in the Cupatitzio River.

Speciation of silversideChirostoma attenuatum(Pisces: Atheriniformes) in Central Mexico

“…In this scenario, the symmetrical migration rates in mtDNA = 0.01 migrants per generation and the asymmetrical migration rates in nDNA Zirahuen‐Patzcuaro = 0.013 versus nDNA Patzcuaro‐Zirahuen = 0.06% migrants per generation between lineages, indicating that the recent connection of the lakes allowed migration but was sufficiently low to maintain genetic differentiation, as is supported by the significant values in Φ st and AMOVA, as well as the haplotype network and species trees. These results support the suggestion that the speciation process is better explained by ecological speciation than by the existence of a barrier, as has been proposed in A. meeki with respect to A. diazi , in which migration was found, but was not significant and was low enough to maintain the genetic differentiation of the species (Corona‐Santiago et al., ).…”

“…This is supported by stratigraphic information (Israde‐Alcántara, Wade, Garduño‐Monroy, & Barron, ), limnologic data (Bradbury, ; Israde‐Alcántara, Garduño‐Monroy, & Ortega, ), and geological evidence (Israde‐Alcántara & Garduño‐Monroy, ). The Patzcuaro and Zirahuen lakes are located in an area of high volcanic activity known as the “Tarasco Corridor,” where more than 1,000 active volcanic cones have been recorded since the Pliocene (Corona‐Santiago et al., ). The volcanic dynamism was produced by tectonic activity that increased in the area ~700,000 years ago (Johnson & Harrison, ; Luhr & Simkin, ), shaping the physiography of the Zirahuen and Patzcuaro basins, and corresponding to the time of the early cladogenetic event.…”

“…These dates are supported by the genetic flow demonstrated in the sister goodeid species A. diazi (Patzcuaro) and A . meeki (Zirahuen; Corona‐Santiago et al., ). In this scenario, the symmetrical migration rates in mtDNA = 0.01 migrants per generation and the asymmetrical migration rates in nDNA Zirahuen‐Patzcuaro = 0.013 versus nDNA Patzcuaro‐Zirahuen = 0.06% migrants per generation between lineages, indicating that the recent connection of the lakes allowed migration but was sufficiently low to maintain genetic differentiation, as is supported by the significant values in Φ st and AMOVA, as well as the haplotype network and species trees.…”

“…This inconsistency could be explained by the formation of Zirahuen Lake via damming of a stream that flowed to Patzcuaro Lake, producing a biogeographic scenario of peripheral isolation. Accordingly, the founder population was low, allowing stochastic processes, such as genetic drift and selection, to occur more slowly in nDNA than in mtDNA (Funk & Omland, ; Zink & Barrowclough, ), influencing the C. zirahuen demographic history (Lacy, ), as was proposed for the A. diazi complex (Corona‐Santiago et al., ). The Bayesian skyline plot showed a population expansion ca .…”

“…Evidence of a secondary paleoconnection, about 8,000 years ago (Garduño‐Monroy et al., ; Israde‐Alcántara et al., ), is supported by phylogeographic findings of the closely related goodeine species Allotoca meeki Álvarez, 1959 from Zirahuen and Allotoca diazi Meek, from Patzcuaro that suggest a recent isolation process ca . 7,000 years ago (Corona‐Santiago, Doadrio, & Domínguez‐Domínguez, ).…”