Progressive colonization and restricted gene flow shape island-dependent population structure in Galápagos marine iguanas (Amblyrhynchus cristatus)

Abstract

Background: Marine iguanas (Amblyrhynchus cristatus) inhabit the coastlines of large and small islands throughout the Galápagos archipelago, providing a rich system to study the spatial and temporal factors influencing the phylogeographic distribution and population structure of a species. Here, we analyze the microevolution of marine iguanas using the complete mitochondrial control region (CR) as well as 13 microsatellite loci representing more than 1200 individuals from 13 islands.

Results: CR data show that marine iguanas occupy three general clades: one that is widely distributed across the northern archipelago, and likely spread from east to west by way of the South Equatorial current, a second that is found mostly on the older eastern and central islands, and a third that is limited to the younger northern and western islands. Generally, the CR haplotype distribution pattern supports the colonization of the archipelago from the older, eastern islands to the younger, western islands. However, there are also signatures of recurrent, historical gene flow between islands after population establishment. Bayesian cluster analysis of microsatellite genotypes indicates the existence of twenty distinct genetic clusters generally following a one-cluster-per-island pattern. However, two well-differentiated clusters were found on the easternmost island of San Cristóbal, while nine distinct and highly intermixed clusters were found on youngest, westernmost islands of Isabela and Fernandina. High mtDNA and microsatellite genetic diversity were observed for populations on Isabela and Fernandina that may be the result of a recent population expansion and founder events from multiple sources.

Conclusions: While a past genetic study based on pure FST analysis suggested that marine iguana populations display high levels of nuclear (but not mitochondrial) gene flow due to male-biased dispersal, the results of our sex-biased dispersal tests and the finding of strong genetic differentiation between islands do not support this view. Therefore, our study is a nice example of how recently developed analytical tools such as Bayesian clustering analysis and DNA sequence-based demographic analyses can overcome potential biases introduced by simply relying on FST estimates from markers with different inheritance patterns.

Figure 1

Bayesian-based phylogeny of Galápagos marine iguanas and distribution of mitochondrial clades based on mtDNA CR data. a) The topology and branch lengths were inferred using the program MRBAYES, but the rooting shown here was inferred using the software BEAST (see Methods). Branch lengths are in number of substitutions per site. Bayesian posterior probability values from MRBAYES are shown supporting the three major clades. b) Map of the Galápagos islands detailing population locations and symbols (details in Table 1). Pie charts illustrate the geographic distribution of the mtDNA CR clades resulting from the analysis of 1203 marine iguanas.

Figure 2

Haplotype network constructed under statistical parsimony for all Galápagos marine iguana mtDNA CR haplotypes. Haplotype numbers are preceded by the letter "H." The smallest circles denote missing haplotypes. The other four circle sizes reflect the number of individuals. In order of increasing area, this corresponds to 1-6, 7-20, 21-50, and 50 or more individuals. All singletons were removed from populations on Fernandina and western Isabela in order to more clearly display the overall phylogeographic patterns. Island distribution of each haplotype is indicated by color according to the embedded legend.

Figure 3

Bayesian mixture analysis. a) Individual-based mixture analysis of 1225 Galápagos marine iguanas to 20 genetic clusters as determined by the program STRUCTURE following the estimation of true number of genetic clusters (K) following [44] Evanno et al. (2005; see Figure S1 [see Additional file 5]). Note that individual samples taken at two different time points (i.e. in 1991/93 and 2004) on an island location represent the same genetic cluster. With the exception of Fernandina and Isabela all major islands each represent a distinct genetic cluster. b) Population-based mixture analysis for the same number of genetic clusters according to STRUCTURE. For (a) and (b) the program DISTRUCT [45] (Rosenberg 2004) was used to generate the display genetic clusters and degree of admixture of individuals.