Measuring dispersal rate in Neotropical fishes in units of ‘wallace’

Portrait of Wallace from his autobiography My Life, Vol. 1 (Chapman and Hall, London, 1905). Copyright © Royal Society.

Portrait of Wallace from his autobiography My Life, Vol. 1 (Chapman and Hall, London, 1905). Copyright © Royal Society.

Alfred Russel Wallace often gets second billing compared to Charles Darwin but in a paper recently accepted at Systematic Biology, Tagliacollo et al.  define a new term for their analyses (dispersal rate, D) and measure D in units of ‘wallaces‘ (wa) to honor the contributions of Alfred Russel Wallace to the field of biogeography.

This detail is a small part of a great paper that tests alternative hypotheses about how freshwater fish assemblages formed in Central America and the Greater Antilles (Cuba, Hispaniola, Puerto Rico, Jamaica, and the Cayman Islands). The authors used parametric biogeographic methods to estimate rates of coordinated dispersal in the two most species clades of freshwater fish in the Caribbean basin- the heroine cichlids and poeciliine live-bearers. Parametric biogeography is a growing field at the intersection of historical biogeography and macroevolution. Its aim is to model the history of range evolutions within a phylogenetic and spatial framework (see Ree & Sanmartín 2009 and Sanmartín 2010).

Specifically, Tagliacollo et al. developed new methods for:

i) measuring macroevolutionary dispersal rates in the context of a landscape with changing paleogeographic interconnections

ii) estimating expected rates of dispersal from paleogeographic considerations of area, river discharge volume, and distance

iii) comparing observed and expected dispersal rate values to identify the relative contributions of these paleogeographic agencies.

For the purposes of this paper, dispersal rate is defined as “the number of biogeographic range expansion events per million years in taxa leaving descendants that persist” to present day. Dispersal refers to the colonization of new areas outside of an established species range. The authors generated phylogenetic trees and estimated divergence times based on multi-locus mitochondrial and nuclear data sets. The absolute divergence times were constrained using information from dated fossils. Next, the authors modified the code of the parametric biogeography program LAGRANGE and estimated observed dispersal rates (Do) from the time-calibrated molecular phylogenies over a paleogeographic landscape. As for the methodological details…

[the modified program, called LAGRANGE+] differs from the original LAGRANGE program in treating each dispersal rate parameter in the dispersal matrix as a separate value to be estimated. The dispersal scalar is removed from the process, and the dispersal matrix is then interpreted as a set of absolute (not relative) dispersal rates. The models of area connectivity through time (Fig. 1, center panel) employ eight independent dispersal rate parameters among five geographic areas and three time intervals.

Tagliacollo et al. developed a dynamic model of Caribbean Plate evolution and estimated Do between five geographic areas (labeled A-E in Fig.1) over three time intervals (I-III in Fig. 1). Expected dispersal rates (De) were generated from nine alternative paleogeographic models with three parameters- dispersal rates were i) proportional to target area,  ii) inversely proportional to distance, and iii) proportional to the volume of freshwater discharge from nearby rivers (for example, the Proto-Orinoco-Amazon River).

Fig. 1. Estimating observed dispersal rates (DO) across the Caribbean Plate margins in LAGRANGE+. Paleogeographic reconstructions (left) and models of area connectivity through time (center), represented as a dispersal rate matrices (right). Dispersal rate parameters (Greek letters) are estimated in a ML framework employing a Dispersal-Extinction-Cladogenesis (DEC) model of geographic range evolution and empirical time-calibrated molecular phylogenies. Time intervals (I-III) encompass major geological events thought to have affected vicariance and dispersal across the Caribbean Plate (see text). Paleogeographic maps and data from Pindell and Kennan (2009) and Blakey (2011). Areas: A = Cis-Andean; B = Trans-Andean; C = Panama; D = Nuclear Central America; E = Greater Antilles.

Fig. 1. Estimating observed dispersal rates (Do) across the Caribbean Plate margins in LAGRANGE+. Paleogeographic reconstructions (left) and models of area connectivity through time (center), represented as a dispersal rate matrices (right). Dispersal rate parameters (Greek letters) are estimated in a ML framework employing a Dispersal-Extinction-Cladogenesis (DEC) model of geographic range evolution and empirical time-calibrated molecular phylogenies. Time intervals (I-III) encompass major geological events thought to have affected vicariance and dispersal across the Caribbean Plate (see text). Paleogeographic maps and data from Pindell and Kennan (2009) and Blakey (2011). Areas: A = Cis-Andean; B = Trans-Andean; C = Panama; D = Nuclear Central America; E = Greater Antilles. Figure and caption from Tagliacollo et al. (2015)

Results! The LAGRANGE+ analyses found a persistent dispersal corridor along the eastern edge of the Caribbean Plate during the Paleogene (66-23 million years ago) with the earliest dispersal of heroine and poeciliine fishes to the Antilles ranging from 48.9-42.6 million years ago and 59.6-49.5 million years ago, respectively.

Do estimates suggested successful colonization from Nuclear Central America (area D in Fig. 1) and Southern Central America (area C) to trans-Andean northern South America (area B). The nine alternative models used to estimate De found high dispersal rates along the eastern margin of the Caribbean Plate and low dispersal along the western margin during the late Upper Cretaceous to the early Paleogene. Of the paleogeographic parameters examined, geographic distance was the single best predictor of Do. These results are “consistent with overseas dispersal by means of rafting on a freshwater plume to the Antilles during the Paleogene, but not to Central America during the Neogene.”

Finally, its not all about the Isthmus-

Phylogenetic and biogeographic data reviewed here suggest the Pleistocene Isthmian exchange was of limited taxonomic scope for freshwater fishes, bidirectional, with taxa moving in both directions, and asymmetrical, with a preponderance of taxa moving south into the Pacific slope of Colombia (Chakrabarty and Albert 2011). The rise of the Isthmus is best viewed as the most recent of many geological and geographic events involved in the formation of the modern Central American and trans-Andean ichthyofaunas. The Isthmus is only one piece of a richly complex puzzle that is the biogeographic history of this region.

  Reference

Tagliacollo, V. A., Duke-Sylvester, S. M., Matamoros, W. A., Chakrabarty, P., & Albert, J. S. (2015). Coordinated Dispersal and Pre-Isthmian Assembly of the Central American Ichthyofauna. Systematic Biology, in press. DOI: 10.1093/sysbio/syv064

About Melissa DeBiasse

I am a postdoctoral researcher at the University of Florida Whitney Laboratory for Marine Bioscience. As an evolutionary ecologist I am interested in the processes that generate biodiversity in marine ecosystems. My research uses experimental methods and genomic and phenotypic data to test how marine invertebrate species respond to biotic and abiotic stressors over ecological and evolutionary timescales.
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