Multi-locus phylogeography of the dusky dolphin ( Lagenorhynchus obscurus ): passive dispersal via the west-wind drift or response to prey species and climate change?(Research article)(Report)

Authors: April D Harlin-Cognato (corresponding author) [1]; Tim Markowitz [2]; Bernd W�rsig [3]; Rodney L Honeycutt [4]

Background

Over a 2.5 million year period in the Pleistocene repeated patterns of expansion and recession of ice sheets from Antarctica influenced globally the distribution of sea surface temperatures and the flow of ocean currents [1, 2, 3]. These historical geological events during the Plio-Pleistocene influenced contemporary patterns of genetic structure observed in marine organisms living in the Southern Hemisphere [4, 5, 6]. For example, small-bodied dolphins of the genera

Cephalorhynchus and Lagenorynchus occupy temperate waters in the Southern Hemisphere and share similarities in their distribution and pattern of morphological and genetic (exclusively mtDNA) divergence that have been interpreted as being the result of dispersal corridors present during inter-glacial periods in the Plio-Pleistocene [7, 8]. These contemporary patterns of divergence and distribution observed for these genera of dolphin inspired the west-wind drift hypothesis, which suggests an eastward dispersal of dolphins via a unidirectional, linear route with the temperate west-wind drift ocean current present during the Plio-Pleistocene. The west-wind drift hypothesis plus the preference for temperate waters purportedly explains the roughly concordant distribution of these dolphins in temperate, upwelling regions along coastal South Africa, South America, and New Zealand within 8[degrees]C and 16[degrees]C isotherms (Figure 1). As a result, the current ranges of these genera are large but discontinuous, separated by vast expanses of ocean and tropical waters between temperate regions.Figure 1: Global distribution of the dolphin genera Lagenorhynchus and Cephalorhynchus and associated prey species in temperate ocean regions . (A) Grey shaded areas outline the distribution of sardines (Sardinops , Sardina ) and anchovy (Engraulis ), which are regionally bounded by the 13[degrees]C and 25[degrees]C isotherms (dotted curves; modified from Grant and Bowen [50]). Coloured areas indicate the distribution of Lagenorhynchus species. Cephalorhynchus distributions overlap partially with Lagenorhynchus species in all areas indicated with an arrow. The distribution of dolphin species with anchovy and sardines is indicated where coloured and grey shaded areas overlap along temperate, coastal regions. (B) The west-wind drift hypothesis suggests that the dusky dolphin (L. obscurus ) dispersed via a circum-global band of uninterrupted cool water, starting in coastal Peru, moving eastward through Drake's passage, to Argentina, South Africa, and New Zealand. [figure omitted]Lagenorhynchus obscurus (the dusky dolphin) is the one of the most widely distributed dolphin species in the Southern Hemisphere, with a disjoint distribution restricted to temperate waters (Figure 1). As such, this species provides a model for testing several predictions explicit in the west-wind drift hypothesis. First, the west-wind drift hypothesis implies a Peruvian origin of the dusky dolphin followed by eastward dispersal to other regions (Figure 1) [7, 9]. In support of this prediction molecular studies have proposed that the Peruvian population was founded when L. obscurus and L. obliquidens , an anti-tropically distributed sister-species pair [10, 11], diverged during a southward equatorial transgression in the Pacific Ocean approximately 1 million years ago when tropical waters cooled [12, 13]. In contrast, recent molecular studies with better geographic sampling and both nuclear and mitochondrial DNA markers indicate a phylogeographic history of the dusky dolphin inconsistent with the west-wind drift hypothesis [8, 14]. These studies suggest an alternative Atlantic/Indian Ocean origin [8], which is inconsistent with an anti-tropical speciation event in the Pacific Ocean and necessitates an alternative explanation for the transition between oceans.

Second, dispersal via the west-wind drift should result in a pattern of genetic variation that is linear and unidirectional [8, 15]. One molecular study [14] suggests that Argentina, South Africa, and New Zealand populations have experienced relatively recent contact, perhaps as a large ancestral Atlantic/Indian Ocean population. Therefore, the origin of the dusky dolphin and its phylogeographic history remain inconclusive.

Finally, west-wind drift represents a passive dispersal mechanism that would result in a distributional pattern of the dusky dolphin that should be independent of changes in sea-surface temperatures, prey distribution, and correlated primary productivity. The dusky dolphin is concentrated in regions of high primary productivity, where cyclic upwelling supports an abundance of schooling anchovy (

Engraulis sp.), sardines (Sardinops sp.), and other small fishes and squid limited in their distribution to temperate regions (Figure 1). The geographic association of these fishes and the dusky dolphin is not coincidental. Stomach-content analysis and behavioral observations in Argentina, Peru, and New Zealand indicate the diet of the dusky dolphin is comprised mainly of these prey items [13, 16], and that movements of dolphin populations are coincident with seasonal shifts in prey distribution [17, 18]. The preference for temperate prey species is an ancestral characteristic of all members of the genus Lagenorhynchus , including the Pacific white-sided dolphin (L. obliquidens ), whose distribution is correlated with that of North Pacific anchovy (Figure 1). Sardines and anchovy are regionally and physiologically bounded by 13[degrees]C and 25[degrees]C isotherms (Figure 1) [4]. Clearly, the phylogeographic history of the dusky dolphin and its temperate prey species are biologically linked, so that global climatic oscillations affecting temperate regions would produce a history correlated with the isolation of ocean basins, with the degree of regional genetic divergence concordant with the closure of temperate ocean corridors and the frequency and duration of fluctuations in sea surface temperatures that altered the distribution and availability of prey.

In this study, we use new nuclear and mitochondrial DNA sequence data and complete geographic sampling to challenge the role that the west-wind drift played in the genetic structuring and dispersal of dusky dolphin populations. We provide a global phylogeographic perspective of the origin of the dusky dolphin, and assess the historical patterns of gene flow related to the location of temperate, up-welling coastal regions that are tightly linked to the distribution of prey species. In contrast to previous studies, our data support an alternative to the west-wind drift hypothesis, with a temporal and environmental correlation between the phylogeographic history of the dusky dolphin, its anchovy prey, and the Plio-Pleistocene paleoceanography of the Southern Ocean and Eastern Equatorial Pacific.

Results

Diversity indices

Table 1 summarizes indices of genetic diversity. With the exception of cyt

b for Peru, haplotype and nucleotide diversity for the cyt b and control region was high. The lower diversity of cyt b in Peru was first described by Cassens et al. [14] and was attributed to high levels of mortality along the Peruvian coastline.Table 1 caption: Summary of genetic diversity indices for cytochrome b , control region, and actin intron I sequence data [table omitted]

Prediction 1: Peruvian origin

The dusky dolphin d-loop and cyt

b haplotype networks recovered a Peru-specific lineage divergent from other geographic regions by several missing intermediate haplotypes (Figures 2 and 3). Similarly, the Bayesian analysis recovered a monophyletic clade of Peruvian haplotypes with 100% posterior probability, and generally supported the phylogenetic pattern of the statistical parsimony networks (Figure 2). The Bayesian analysis indicated with 96% posterior probability that the root of the dusky dolphin phylogeny was not the Peruvian clade, but rather occurred along a lineage of South American and New Zealand haplotypes (Figure 2).Figure 2: The statistical parsimony network of dusky dolphin cytochrome …