Phylogeography of Seaweeds in the South East Pacific: Complex Evolutionary Processes Along a Latitudinal Gradient

  • Marie-Laure Guillemin
  • Myriam Valero
  • Florence Tellier
  • Erasmo C. Macaya
  • Christophe Destombe
  • Sylvain Faugeron


The coast along the temperate South East Pacific (SEP) presents a simple linear topography with a north-south orientation spanning more than 4600 km. However, environmental heterogeneity associated with two major biogeographic boundaries has been described along the SEP (30–33°S and 42°S). Recent phylogeographic studies of seaweeds revealed the existence of different cryptic species along the SEP coast and that most of the genetic breaks between them are broadly congruent with the biogeographic boundaries. These phylogeographic patterns characterized by genetic discontinuities could be attributed to historical vicariance or to budding speciation. For SEP seaweeds, two major phylogeographic patterns are observed. Endemic species living north of 42°S show complex haplotype networks and an almost complete genetic isolation between populations located only a few kilometres from each other. This extreme genetic patchiness has been related to the combined effects of limited dispersal, reduced population size and high population turnover of these intertidal seaweeds due to stochastic effects of climatic and tectonic catastrophes. On the other hand, species with a range distribution limited to the south of 42°S and inhabiting the area highly affected by the coastal ice cap during the Last Glacial Maximum (LGM), show typical signatures of post-glacial demographic expansion. Finally, molecular studies reveal that several species are recent immigrants from New Zealand, demonstrating the importance of oceanic dispersal in shaping the diversity of the SEP.


Biogeographic boundaries Budding speciation Chile Cryptic species Phylogeographic breaks Post-glacial recolonization 

10.1 Introduction

The temperate South East Pacific (SEP) represents one of the most productive marine ecosystems of the world. Research interest in this region has increased during the recent years and consequently, phylogeographic studies have started to accumulate at a rapidly increasing rate. Areas of research range from simple exploratory analyses of genetic variation focusing on the identification of genetic resources, to specific assessments of the role of biogeographic discontinuities in the evolutionary history of an organism. Most studies are based on a ‘single marker-single species’ sampling design and focus on different areas of the SEP which have limited the description of general genetic trends in the region. Indeed, some studies reveal strong genetic structure and have stated that highly regionalized historical and contemporary factors are driving these patterns (see, for example Tellier et al. 2009; Fraser et al. 2010a; Brante et al. 2012; Montecinos et al. 2012; Varela and Haye 2012), whereas other studies suggest that species form single genetic units that share a common demographic history (for examples see Cárdenas et al. 2009; Haye et al. 2010, 2012). Recently, the first multispecies comparative study was conducted in central and northern Chile to investigate the role of oceanographic and biogeographic boundaries present around 30°S (Haye et al. 2014). This study suggests that genetic structure among populations in eight marine invertebrate species can be largely explained by dispersal potential and historical processes that limit gene flow near 30°S (Haye et al. 2014). Indeed, species with short pelagic larval duration display a clear-cut phylogeographic discontinuity coincident with the biogeographic transition zone at 30°S whereas the species with long-term pelagic stage do not show a genetic discontinuity. Another biogeographic boundary described at 42°S (Camus 2001) was also reported to match the location of genetic discontinuities (i.e. cryptic species were defined on the both sides of the 42°S; Fraser et al. 2009). Along the SEP, the concordance between biogeographical boundaries and genetic breaks has been attributed to historical vicariance caused by oceanographic or climatic features (Tellier et al. 2009; Zakas et al. 2009; Brante et al. 2012; Montecinos et al. 2012; Varela and Haye 2012; Haye and Muñoz-Herrera 2013; Haye et al. 2014).

The use of molecular markers has allowed for the identification of many cryptic species in marine organisms. Molecular identification has been especially useful for studying organisms, such as seaweeds, that display few diagnostic characters and are morphologically simple (Leliaert et al. 2014). The lack of morphological characteristics that differ between evolutionary units (i.e. species as defined by the lineage species concept) has for some time obscured the study of biogeographic boundaries, species distributions, and speciation processes in seaweeds. For example, in a molecular study of the red alga Portieria hornemannii in the Philippine archipelago, Payo et al. (2013) demonstrates that this unique morphospecies is in fact composed of 21 cryptic taxa. These remarkable findings led to the complete reinterpretation of Portieria’sbiogeography in the region. Even if many cryptic species have been reported in marine algae along the SEP, the general processes that contribute to speciation and genetic breaks, and how these relate to biogeographic boundaries and vicariance, have not yet been investigated for these organisms.

In this chapter, we intend to discuss new findings of seaweed phylogeographic structure and cryptic sister species distributions along the SEP to gain some biogeographic insight and to identify some of the major drivers of evolutionary processes that have affected Chilean seaweeds.

10.2 Major Biogeographical Characteristics of the SEP Coast: Linear Gradient or Strong Regional Pattern?

The SEP coast (from ca. 14°S to 56°S) is characterized by a linear topography with a north-south orientation spanning more than 4600 km (Fig. 10.1). From southern Peru (i.e. 18°S) to the Island of Chiloé (i.e. 42°S), the coastline is straight and continuous and presents no major topographic discontinuities except for a few relatively small open bays. South of Chiloé Island, the topography differs greatly, being dominated by insular systems surrounded by numerous fjords and channels (Thiel et al. 2007). The oceanic circulation of the SEP is dominated by the northward flowing Humboldt Current (HC) that extends to 5°S where it meets the Equatorial front, and by the southward flowing Cape Horn Current (CHC; Strub et al. 1998; Fig. 10.1a). Both circulation features originate between 40°S and 45°S where the Antarctic Circumpolar Current (ACC) approaches South America. The northern latitude at which the ACC meets the continent shifts seasonally from 35–40°S during austral winter to 45°S during austral summer (Thiel et al. 2007). The direct influence of the Humboldt Current system promotes upwelling of cold and nutrient-rich waters to coastal ecosystems (Hormazabal et al. 2004; Thiel et al. 2007). This peculiarity favours primary productivity (Lachkar and Gruber 2012) even at low latitudes, as far north as 5°S off the coast of Peru, and is thus a major determinant of marine species’ latitudinal ranges.
Fig. 10.1

Map of the coastal South East Pacific (SEP) at present time (a) and reconstruction of the Quaternary environmental changes in the region (b). Present time map shows the three marine biogeographic provinces (after Camus 2001) with grey shaded lines representing the reported biogeographic breaks around 30–33°S and 42–43°S. Mean annual sea surface temperatures (i.e. SST, dashed lines, Locarnini et al. 2010), the directions of the major surface currents (grey arrows, Kaiser et al. 2005: Antarctic Circumpolar Current (ACC), Humboldt Current (HC), Cape Horn Current (CHC)) and the position of the Subantarctic Front (SAF) and the Antarctic Polar Front (APF) (after Belkin and Gordon 1996) are indicated. A sketched reconstruction of the Last Glacial Maximum (LGM) environmental changes in the region shows an estimated extension of the ice sheet (McCulloch et al. 2000), the latitudinal shift of the major surface currents and SST (modified after Kaiser et al. 2005), the shift in the SAF and APF position (after Verleye and Louwye 2010) and the changes in the coast line occurring in Patagonia during this period (Ponce et al. 2011)

Based partly on these contrasting topological and oceanic characteristics, several studies have proposed the existence of two main biogeographic provinces along the SEP: the Peruvian and Magellan provinces (Camus 2001; Thiel et al. 2007, and references therein; Fig. 10.1a). The Peruvian province is characterized by the presence of a strong tropical component in both its flora and fauna while there is a predominance of species of subantarctic origin in the Magellan province. An Intermediate Area that combines mixed components of the two neighbouring provinces extends from 30–33°S to 42°S (Camus 2001; Thiel et al. 2007). The southern limit of the Peruvian province at 30–33°S is considered to be a major transition zone in the oceanographic features, with strong but seasonal upwelling south of this limit and weak but persistent upwelling conditions in the north (Broitman et al. 2001; Thiel et al. 2007; Tapia et al. 2014). Fenberg et al. (2015) have shown that upwelling-related variables are the best overall predictors of biogeographic structure of northeast Pacific rocky intertidal species, and upwelling seems to be especially influential on assemblages of algae and invertebrates with low-to-medium dispersal capabilities. In this context, it is interesting to note that spatial heterogeneity in the upwelling regime seems to be a major determinant of biogeographic boundaries in the SEP. A second major habitat discontinuity at 42°S, linked with differences in topography, freshwater input, and current dynamics, determines the northern limit for the Magellan province (Brattström and Johanssen 1983; Fernández et al. 2000; Camus 2001; Thiel et al. 2007) (Fig. 10.1a).

The SEP biogeographic boundaries are well correlated with present-day oceanographic conditions but these have not been fully persistent throughout evolutionary history (Fig. 10.1b). However, despite climatic and oceanographic fluctuations, the regions of both 30–33°S and 42°S also represented major habitat discontinuities in the past. First, the northernmost limit of the coastal ice sheet during the Last Glacial Maximum (LGM, 0.026–0.019 Ma) was established near 42°S (McCulloch et al. 2000; Fig. 10.1b). It is well accepted that no coastal ice formed north of that latitude, where potential refugia are proposed for cold-water species. Models of ice sheet extension propose that the southernmost tip of South America, near Cape Horn, was also free of coastal ice and provided the second glacial refugium for marine species of the Magellan province (Hulton et al. 1994, 2002). Indeed, many seaweeds are endemic to the Strait of Magellan, the Beagle Channel, and the Cape Horn archipelago (53–55°S) and are completely absent from the rest of the Magellan province (reviewed by Fernández et al. 2000; Santelices and Meneses 2000). Second, the Intermediate Area experienced historical changes in habitat quality. During glacial periods, the influence of the ACC shifted towards the north leading to a northward shift of the Humboldt/Cape Horn current split (Fig. 10.1b). This change in oceanic circulation likely caused a strong reduction in upwelling in the Intermediate Area, as shown by a reduction of plankton deposits in the region associated with the LGM (Mohtadi and Hebbeln 2004; Kaiser et al. 2005; Verleye and Louwye 2010). In contrast, the area north of 30–33°S is considered to be an area with long-term persistence of upwelling (Mohtadi and Hebbeln 2004).

In addition to the historical geographic and climatic barriers in this region, short-term environmental disturbances have also been taken place repeatedly throughout the SEP’s history. Two major factors have been shown to cause such disturbances. First, the El Niño–Southern Oscillation (ENSO) events that consist of a 2–7 years alternation of a cold period (La Niña) and a warm period (El Niño) (Tarazona and Arnzt 2001). ENSO fluctuations began during the Holocene (Moy et al. 2002) and have intensified during the last 5000–3000 years. El Niño events produce strong mortality in seaweeds due to abrupt increases in the temperature of coastal waters and decreases in nutrient concentrations along the northern part of the SEP, from 6°S to ~30°S (Camus 1990; Martínez et al. 2003). Second, tectonic activity also causes strong seaweed mortality along the extensive coastline of the SEP. Specifically, the sudden coastal up-lifts and downward drops of several meters during major earthquakes, accompanied by major tsunamis, are detrimental to coastal seaweeds (Darwin 1839; Castilla 1988; Castilla et al. 2010; Jaramillo et al. 2012). Several of these coastal up-lifting events have been reported in recent decades and their effects on intertidal communities have been well described (Castilla 1988; Castilla et al. 2010; Jaramillo et al. 2012; Fuentes and Brante 2014; Hernández-Miranda et al. 2014; Ortega et al. 2014).

10.3 Phylogeography: The Problem of Cryptic Species and Consequences for the Delineation of Species Range Distributions

The SEP region hosts nearly 600 seaweed morphospecies of which about 27 % are endemic (Meneses and Santelices 2000). While global diversity gradients for a wide range of taxa follow a classic latitudinal pattern, characterized by a decrease in richness from the tropics to the poles, seaweed morphospecies richness tends to increase with latitude along the SEP (Santelices 1980; Santelices and Marquet 1998; Ramírez 2010; Keith et al. 2014). This inverted latitudinal seaweed diversity pattern, which exists worldwide (Kerswell 2006), was recognized recently by Keith et al. (2014) as a potential consequence of niche conservatism (Pyron and Burbrink 2009). Indeed, contrary to the majority of taxa, macroalgae originating in temperate zones and may have been limited in their ability to colonize tropical regions due to competition with established corals and predation by herbivores (Keith et al. 2014). Along the SEP, the high diversity of seaweeds at high latitudes has been linked to the presence of a highly diverse subantarctic flora with a range distribution that is restricted to the tip of South America (Santelices 1980; Santelices and Marquet 1998; Ramírez 2010). Based on clustering of the flora, Santelices (1980) distinguished three distinct areas along the coastline: the tropical area of northern Peru (4–5°S), a broad intermediate area (5°–53°S) and the southern tip of South America (53–55°S). Within the broad intermediate area, both brown and red seaweeds show clear biogeographical breaks at 30–33°S and 42–43°S (Meneses and Santelices 2000). The dominance of endemic species diminishes southward as they are replaced by subantarctic species, which are distributed in the cold waters of the South Pacific and the Southern Ocean (Santelices 1980).

Species richness along the SEP has probably been underestimated in the above cited studies as species determination was based solely on the use of morphological characters. The development of molecular genetic tools over the past two decades has strongly demonstrated our inability to correctly identify species on the basis of morphological characters alone. Using molecular markers, the presence of cryptic species has been revealed in many taxonomic groups and in various habitats (e.g. in marine environments Knowlton 1993, 2000; and in particular, in algae, see the recent review Leliaert et al. 2014). Studies based on molecular markers have accumulated compelling evidence that algal names have been applied incorrectly and morphological identification could lead to erroneous conclusions about trait evolution in seaweeds (see, for example the comparative analysis of chemical defence in Gracilariaceae, Weinberger et al. 2010). These erroneous taxonomic assignments have also revealed that seaweeds could have higher species diversity, and species could be more regionally confined than previously thought (see for example Tronholm et al. 2012; Payo et al. 2013; Pardo et al. 2014; Vieira et al. 2014).

Along the SEP, molecular studies have revealed the presence of cryptic/sister species in both red and brown seaweeds (see Table 10.1), and new species have recently been described in the region. For example, Lessonia berteroanaand Lessonia spicata now stand in for the well studied morpho-species Lessonia nigrescens in the central and northern part of the SEP (González et al. 2012). Similarly, the species Pyropia columbina reported to be one of the most common and ubiquitous bladed Bangiales in the Southern Pacific is now restricted to a subantarctic range, while new endemic species were described for the temperate coast of New Zealand (Pyropiaplicata, Nelson 2013) and Chile (P.orbicularis, Ramírez et al. 2014). Several new taxa yet unnamed were identified based on phylogenetic and phylogeographic studies of Ectocarpus (Peters et al. 2010), Durvillaea (Fraser et al. 2009, 2010a), Adenocystis (Fraser et al. 2013), Mazzaella (Montecinos et al. 2012) and Nothogenia (Lindstrom et al. 2015) (Table 10.1).
Table 10.1

Summary of phylogeographic studies of seaweed taxa along the South East Pacific coast

Sampling range, habitat, life-history, molecular data available and reference are given for each taxon. The name of the morpho-species for which the studies were undertaken is given in the second column. The species and taxa including extended geographical coverage and population sampling design are shaded in light grey. Abbreviationscox1: cytochrome c oxidase subunit I, cox2–3: intergenic sequence between the cytochrome c oxidase subunit II and III, atp8/trnS: intergenic sequence between the ATPase subunit 8 gene and the trnS, ITS: internal transcribed spacer, psbA: photosystem II thylakoid membrane protein D1, rbcL: large subunit of the Rubisco; RuBisCo spacer: intergenic sequence between the large and the small subunits of Rubisco, SSU: Small subunit rRNA gene; [M] mitochondrial, [C] chloroplastic, [N] nuclear

aPart of the data set was obtained using single-strand conformation polymorphism (SSCP)

Interestingly, molecular data seem to strengthen the existence of the biogeographic boundaries proposed by Meneses and Santelices (2000) for seaweeds. Indeed, the genetic breaks found between Durvillaea antarctica “central Chile” and D. antarctica “subantarctic”, between Mazzaella laminarioides “north” and M. laminarioides “center” and between L. berteroana and L. spicata are broadly congruent with the 42–43°S and the 30–33°S biogeographic boundaries (Table 10.1; Fig. 10.2). For other taxa studied, the lack of extensive sampling does not allow a clear pinpointing of the location of the phylogeographic breaks. However some clades, such as Adenocystis utricularis “Clade 3-COI” (Fraser et al. 2013) or Nothogenia “Taxon A” and “Taxon B” (Lindstrom et al. 2015), seem to be restricted to the Intermediate Area (Table 10.1). Finally, molecular studies have revealed that numerous species are shared between the SEP and New Zealand, the Subantarctic Islands and the Falkland Islands (in the genera Macrocystis, Macaya and Zuccarello 2010a, b; Durvillaea, Fraser et al. 2009, 2010a; Adenocystis Fraser et al. 2013; Gigartina, Billard et al. 2015; Gracilaria, Guillemin et al. 2014; Nothogenia, Lindstrom et al. 2015; Capreolia, Boo et al. 2014; Bostrychia, Fraser et al. 2013). These results demonstrate the importance of oceanic dispersal in shaping the diversity of the SEP, especially in the Magellan province and in the Intermediate Area.
Fig. 10.2

Schematized median joining haplotype networks of 10 seaweed taxa along the South East Pacific coast for which extensive phylogeographic studies have been published (see Table 10.1). Range distribution of each taxon is represented by a grey box (for more information about latitudinal limits of each taxon see Table 10.1). In all haplotype networks each circle represents a haplotype and, while the sizes of circles are proportional to haplotype frequencies in each taxon, they are not comparable across studies. Black lines represent mutational steps between haplotypes and the length of each line is proportional to the number of different base pairs between them. For more information about each taxon see Table 10.1

Although the sample sites, sample sizes and level of diversity differ among taxa (Table 10.1), two major phylogeographic structuring patterns can be observed (Fig. 10.2). While endemic species living north of 42°S show complex reticulated haplotype networks, species that have recently colonized the SEP or endemic species with a range distribution limited to the south of 42°S generally show simple star-like haplotype networks (Fig. 10.2). Because these differences reflect distinct evolutionary trajectories and demographic histories, in the following sections, we discuss the historical and contemporary scenarios that likely shaped these different patterns of phylogeographic structure.

10.4 Parapatric Distribution and Speciation Processes Along a Linear Coast

As 42°S is considered to be the northern limit of the coastal ice cap (McCulloch et al. 2000; Fig. 10.1b), comparing the phylogeography of seaweeds endemic to the SEP that are distributed north of 42°S allows for the inference of historical processes that occurred along this coast long before the LGM. We will focus on three case studies of previously recognized morphospecies distributed in the Intermediate Area and/or the Peruvian Province (Lessonia nigrescens, M. laminarioidesand Durvillaea antarctica) that were in fact proven to include divergent taxa or crypticsister species (Table 10.1; Figs. 10.2 and 10.3).
Fig. 10.3

Growth habits, schematic representation of published phylogenetic trees and range distribution of Lessonia berteroana and L. spicata, Durvillaea antarctica “central Chile” and D. antarctica “subantarctic” and Mazzaella laminarioides “north”, M. laminarioides “center” and M. laminarioides “south.” For L. berteroana and L. spicata phylogenetic trees were retrieved from Tellier et al. (2009) using fast evolving atp8/trnS (mitochondrial) and ITS1 (nuclear) markers and slow evolving ITS2 (nuclear) and RuBisCo spacer (chloroplast) markers. For D. antarctica a phylogenetic tree for all four concatenated markers (mitochondrial: COI, chloroplast: rbcL and nuclear: 18S rRNA and 28S rRNA) was retrieved from Fraser et al. (2010b). For M. laminarioides phylogenetic trees were retrieved from Montecinos et al. (2012) using the fast evolving COI (mitochondrial) marker and slow evolving rbcL (chloroplast) marker. Distributions of cryptic species or lineages are based on the work of Tellier et al. (2009, 2011a) for L. berteroana and L. spicata, on the work of Fraser et al. (2009, 2010a, b) for D. antarctica “central Chile” and D. antarctica “subantarctic” and Montecinos et al. (2012) for M. laminarioides “north”, M. laminarioides “center” and M. laminarioides “south”. Photos represent, from top to bottom, thalli of L. berteroana growing in the wave-swept intertidal zone in Los Verdes, Iquique (20°25′S, photo E. Macaya), thalli of D. antarctica “central Chile” in Mar Brava (41°52′S, photo E. Macaya) and thalli of M. laminarioides “south” growing in the high intertidal zone in Caleta Hiuro, Valdivia (39°57′S, photo M-L. Guillemin)

10.4.1 Cryptic Phylogenetic Species Within Previously Reported Morphospecies: Phylogenetic Breaks that Do not Always Fit the Biogeographical Boundaries

The endemic red alga M. laminarioides dominates the middle-high intertidal rocky shore while the kelps L. nigrescens and D. antarctica are found in wave-swept low intertidal areas. Both M. laminarioides and L. nigrescens morphospecies, considered poor dispersers (Santelices 1990), show genetic differentiation at short geographic distances (hundreds of meters to a few kilometres, Faugeron et al. 2001, 2005; Tellier et al. 2011a). Conversely, the bull kelp D. antarctica, characterized by a buoyant thallus is considered to be a good disperser through rafting (Fraser et al. 2009, 2010a, b; also see chapters by Macaya et al. 2016 and Fraser 2016 in this volume).

Despite ecological differences among these morphospecies, molecular studies have revealed that each is subdivided into phylogenetic species, i.e. reciprocally monophyletic and highly divergent clades (see Fig. 10.3). Two clades were recovered for L. nigrescens (Tellier et al. 2009), whereas three clades were recovered for M. laminarioides (Montecinos et al. 2012). D. antarctica is a species complex of four deeply divergent taxa, of which only two are present along the SEP coast (i.e. “central Chile” and “subantarctic”, Fraser et al. 2010a, b).Within each morphospecies, molecular markers were congruent in revealing the occurrence of cryptic species distributed in parapatry along the SEP coast (Figs. 10.2 and 10.3). The location of phylogeographic discontinuities are specific to each morphospecies: 30°S for L. nigrescens, 33°S and 38°S for M. laminarioides, and in-between 44°S and 49°S for D. antarctica. Interestingly, speciation processes seem to be tightly linked to the processes driving the biogeographic discontinuities. In L. nigrescens and D. antarctica and between M. laminarioides “north” and “center” lineages, genetic discontinuities broadly match the biogeographic boundaries (Meneses and Santelices 2000; Camus 2001; Thiel et al. 2007), which is also the case for several invertebrate species (Brante et al. 2012 Varela and Haye 2012; Haye et al. 2014). However, the genetic break between M. laminarioides “center” and “south” lineages is located between 37°S and 39°S, a region where neither a biogeographic boundary nor a phylogeographic break has been described. The absence of a precise estimate of mutation rates makes it difficult to use molecular clocks to assess the time of divergence among lineages of seaweeds. An exploratory estimation of the historical events at the origin of the divergence among lineages has however been attempted. The separation between M. laminarioides “north” and “center” and between M. laminarioides “center” and “south” were estimated to be between 1.0 and 12.1 Myr and between 0.5 and 5.8 Myr, respectively (Montecinos et al. 2012). The separation between the cryptic species of L. nigrescens (i.e. L.berteroana and L. spicata; González et al. 2012) is estimated to have occurred more recently, between 0.2 and 1.7 Myr (Tellier et al. 2009) and 2.0 and 3.1 Myr (Martin and Zuccarello 2012) depending on the method of estimation. Within D. antarctica, most of the genetic diversity is found around New Zealand where a late Miocene/Pliocene radiation occurred between 1.3 and 9.7 Myr (Fraser et al. 2010b). Even if substantial uncertainty is associated with the timing of lineage splits in the three study cases, the authors agree that they predate Pleistocene glaciations. Because the location and putative timing of the phylogeographic breaks are not fully congruent between taxa, it is not possible to identify specific historical events that may have driven speciation in these intertidal seaweeds (Avise et al. 1987).

In the case of D. antarctica, phylogenetic reconstruction indicates an ancient split of the “central Chile” lineage (Fraser et al. 2009, 2010b) that could have occurred after the first transoceanic dispersal event of the algae from New Zealand, where the genus originates. This allopatric divergence took place well before the diversification of New Zealand taxa from which evolved the “subantarctic” lineage present in Chile (Fraser et al. 2010b). The presence of the “subantarctic” lineage in Chile has been explained by recent, post-glacial transoceanic dispersal from New Zealand and colonization of Patagonia soon after melting of the coastal ice sheet (Fraser et al. 2009, 2010a, b). Therefore, in the case of D. antarctica, the genetic break observed in the SEP around 44–49°S results from a secondary contact between two lineages that have diverged in allopatry on either side of the Pacific Ocean.

Conversely, allopatric speciation has not been proposed as the cause of lineage splitting in either M. laminarioides or L. nigrescens. The genus Lessonia is distributed throughout both New Zealand and Chile, but studies have clearly indicated that divergence between L. spicata and L.berteroana occurred in Chile (Tellier et al. 2009; Martin and Zuccarello 2012). A similar situation has been suggested for M. laminarioides, which is endemic to Chile. While incomplete lineage sorting due to the presence of ancestral haplotypes has been revealed using slow evolving molecular markers, reciprocal monophyly has been systematically observed using faster evolving markers for cryptic lineages of M. laminarioides and for both L. berteroana and L. spicata (Fig. 10.3). The topology of phylogenetic trees built from slow evolving markers was similar for both Mazzaella and Lessonia, with monophyletic derived lineages embedded within a basal polytomy formed by the more ancestral haplotypes (Fig. 10.3). These slow evolving marker tree topologies have been described as a typical signature of budding/peripatric speciation rather than vicariant speciation (Funk and Omland 2003; Crawford 2010). For both the lineage splitting within M. laminarioides and the divergence between L.berteroana and L. spicata, authors have suggested the existence of budding speciation with a sudden expansion at the range limit of the ancestral lineages (Tellier et al. 2009; Montecinos et al. 2012). However, there is a difference in the direction of the range expansion of these ancestral lineages. A range expansion of L. spicata in the area located north of the 30°S could be at the origin of L. berteroana. In contrast, range expansion of M. laminarioides “north” in the area located south of the 33°S could be at the origin of M. laminarioides “center” and “south” (Fig. 10.3; see Tellier et al. 2009; Montecinos et al. 2012 for more details).

Budding speciation (also known as peripatric speciation) was first defined by Mayr (1954) as a speciation process by which an initially small colonizing population becomes reproductively isolated from a species with a larger range. In a paper entitled “Rethinking classic examples of recent speciation in plants”, Gottlieb (2004) developed the argument that this process of speciation in which species ‘bud off’ from ancestral species via small, locally isolated peripheral populations is probably common in plants. In addition, Gottlieb (2004) highlights that recently diverged sister species, for which the overall genetic distance is minimal and the direction of evolution is clear are particularly relevant cases to study this mode of speciation. Many authors have thus argued that budding speciation has a unique signature that, early in the speciation process, sister species should have overlapping or adjacent ranges with very different sizes (i.e. asymmetric ranges) and different realized niche breadths (Funk and Omland 2003; Gottlieb 2004; Grossenbacher et al. 2014; Anacker and Strauss 2014). The prediction of a greater range asymmetry between younger versus older sister pairs was verified recently in two large-scale analyses in plants (114 species of Mimulus sampled in North America, Grossenbacher et al. 2014; 71 sister species from 12 families sampled in the California Floristic Province, Anacker and Strauss 2014). Supporting a scenario of budding speciation, strong ecological niche differences were observed between L. berteroana and L. spicata, including temperature responses (Oppliger et al. 2011, 2012; Vieira et al. 2015), tolerance to air exposure (López-Cristoffanini et al. 2013) and differences in phlorotannin pigments and chlorophyll a fluorescence of PSII (Koch et al. 2015). Niche preferences have yet to be studied for the three lineages of M. laminarioides. The comparison of range sizes of derived and ancestral cryptic species does not seem to fit the prediction of range asymmetry for sister lineages and crypticspecies along the SEP. Indeed, L.berteroana and L. spicata have a very similar range size of about 1500 km which overlaps less than 200 km between 29°S and 30°S (Tellier et al. 2009, 2011a) (Table 10.1; Figs. 10.2 and 10.3). Similarly, the range size of the ancestral northern lineage of M. laminarioides (415 km) is smaller than that of the derived lineages; particularly, the southern lineage is much larger (“central” lineage range of 730 km; “south” lineage range of 2400 km; Table 10.1; Figs. 10.2 and 10.3; Montecinos et al. 2012). The unexpectedly large size of the recently diverged lineages in Mazzaella and Lessonia could be explained by recent post-speciation range shifts that do not reflect the historical range sizes of the lineages during the budding speciation process. Indeed, in the case of M. laminarioides, the “south” lineage has clearly been subjected to successive periods of range expansion/contraction during the glacial periods, which was not the case for the other two lineages that were located north of the glacial coverings (Montecinos et al. 2012). On the other hand, in plants for which clear evidence of range asymmetries support a scenario of budding speciation, the time of divergence between those sister species was determined to be very recent (less than 1 Myr, see for example Baldwin 2005 and Crawford et al. 2006). This does not seem to be the case for the studied seaweeds, and therefore current sister lineage distributions do not necessarily represent the range at budding speciation time for Mazzaella or Lessonia.

10.4.2 Genetic Diversity and Structure Within SEP Endemic Taxa

In order to study patterns of intraspecific genetic variation, we calculated average per population gene diversity (H) and population-pairwise ΦST (Fig. 10.4) using the data published for L. berteroana, L. spicata (Tellier et al. 2009), M. laminarioides “north”, M. laminarioides “center”, M. laminarioides “south” (Montecinos et al. 2012) and D. antarctica “central Chile” (Fraser et al. 2010a). Two contrasting patterns of genetic differentiation were found (Fig. 10.4). On one hand, M. laminarioides “center” and “south” displayed the lowest values of ΦSTST = 0.49 and ΦST = 0.36, respectively), and were composed of haplotypes shared among neighbouring populations. On the other hand, the other four taxa were characterized by low diversity within populations (mean H < 0.2) and high levels of genetic differentiation (mean pairwise ΦST > 0.80). Within these four taxa each haplotype was restricted to a single population or at most to a few close-by populations. The extreme case of such a patchy distribution of haplotypes with almost every population composed of a unique haplotype (mean H close to 0, and ΦST close to 1) was found in the northernmost species L.berteroana (Fig. 10.4). In the same way, no haplotypes were shared between populations of M. laminarioides “north” (Montecinos et al. 2012).
Fig. 10.4

Average gene diversity per population (H) and population-pairwise ΦST calculated within each taxon of Mazzaella laminarioides and for Durvillaea antarctica “central Chile”, Lessonia berteroana and L. spicata. Mean ±95 % confidence intervals are shown. Range distribution is given for each taxon (for more information about latitudinal limits of each taxon see Table 10.1, Montecinos et al. 2012; Fraser et al. 2010a; Tellier et al. 2009, 2011b)

Regardless of the taxa studied, genetic differentiation was significant, confirming that seaweeds are generally poor dispersers compared to other marine organisms. Genetic estimates of dispersal distance in seaweeds are generally considered to be lower than 10 to 50 km (see reviews by Kinlan and Gaines 2003; Valero et al. 2011; Durrant et al. 2014). The minimum values of pairwise ΦST, observed for M. laminarioides “south”, were similar to values observed along the SEP coast for invertebrates with low dispersal capabilities (Haye et al. 2014). If dispersal is the main cause of the observed patterns of genetic differentiation, we would expect to find a significant relationship between genetic distances and geographic distances. Surprisingly, this was not the case for the three taxa of M. laminarioides studied, while isolation-by-distance (IBD) was significant for the three other taxa. For L. berteroana, L. spicata, M. laminarioides “north” and D. antarctica “central Chile” there is almost complete genetic isolation among populations separated by at most a few kilometres or tens of kilometres. It is probable that isolation-by-distance occurs at much shorter spatial scales than the species considered for the phylogeographic studies in these taxa.

The occurrence of haplotypes restricted to a few neighbouring populations and distributed in strict parapatry suggests that mechanisms other than limited dispersal may have contributed to such a patchy genetic diversity pattern. The mid to low intertidal habitat occupied by each of the studied species is intrinsically patchy since rocky shores along the SEP coast are interrupted by influential barriers, such as estuaries or sandy beaches (Thiel et al. 2007). Moreover, strong genetic drift is expected when populations are small and/or experience highly dynamic demographics and pass through periods of reduced population size. The combination of isolation and drift is strongly correlated with the level of genetic differentiation between pairs of populations in D. antarctica (Fraser et al. 2010a). In addition, strong demographic bottlenecks or local extinctions often occur in the region of the SEP located between 30°S and 40°S due to the recurrent effects of El Niño (Martínez et al. 2003; Thiel et al. 2007) and tectonic activity, which cause sudden changes to the elevation of the coast (Castilla 1988; Castilla et al. 2010; Jaramillo et al. 2012). If a local bottleneck is sufficiently strong, population recovery may be achieved by a reduced number of reproductively successful survivors or founders (in the case of local extinction). Such population dynamics typically reinforce the effects of genetic drift and may significantly contribute to patterns of genetic diversity and structure. The combined effects of reduced population size and high population turnover have been shown to reduce local genetic diversity and increase population genetic differentiation (Walser and Haag 2012). These effects can be observed even in species with high dispersive abilities such as floating seaweeds capable of rafting or species with long-lived spores. Considering gene flow restrictions when population densities reach a maximum, the Monopolization Hypothesis (De Meester et al. 2002; Waters et al. 2013) predicts that space will be saturated with local propagules soon after a bottleneck or a founder event, and this will give little chance for settlement of future immigrants. Under this hypothesis, dispersal is less efficient when patches of organisms are dense (Tellier et al. 2011a; Neiva et al. 2012 and for review see Waters et al. 2013). Moreover, the monopolization effect limits immigration therefore reinforcing local adaptation even if environmental heterogeneity in the system is minimal (De Meester et al. 2002). Under this scenario, historical phylogeographic disjunction patterns may last for long periods of time and can lead to speciation.

10.5 Post-glacial Histories: Distinguishing Between Local Population Recovery and Trans-oceanic Introductions

The phylogeographic literature on Patagonian species (i.e. south of 42°S) indicates complex and unexpected evolutionary histories. For terrestrial species, the high genetic diversityoften observed in Patagonia and the strong divergence among populations suggests ancient evolutionary processes that took place long before the LGM. Generally, it is proposed that populations persisted in different refugia in or around the glaciated region during the LGM (see Sérsic et al. 2011 for a review of 33 terrestrial plant and vertebrate species). Freshwater and marine animals seem to follow the same pattern. The use of periglacial refugia is hypothesized for frogs (Nuñez et al. 2011), fish (Ruzzante et al. 2008) and marine gastropods (Sánchez et al. 2011; González-Wevar et al. 2012) whereas glacially embedded refugia are hypothesized for fish (Zemlak et al. 2010), crabs (Xu et al. 2009) and river otters (Vianna et al. 2011).

In contrast, all the seaweed species studied to date show clear phylogeographic signatures of recent, post-glacial expansions in Patagonia. While haplotype networks are generally diversified and complex north of 42°S, only one or very few haplotypes have been detected in the region covered by the Patagonian ice sheet during the LGM (Fig. 10.2). A single haplotype is found in this region for the giant kelp Macrocystis pyrifera (Macaya and Zuccarello 2010a, b) and for the bull kelp D. antarctica (Fraser et al. 2009, 2010a, b), and a star-like haplotype network is observed in the red algae Gigartinaskottsbergii (Billard et al. 2015) and M. laminarioides “south” (Montecinos et al. 2012). It has generally not been possible to precisely estimate the timing of these demographic expansions due to a lack of accurate mutation rates for most molecular markers in seaweeds. However, the single haplotype shared by D. antarctica individuals found among all of the subantarctic islands and continental region of South America matches the latitudinal limits of coastal ice sheet coverage during the LGM (Fraser et al. 2009). This strongly suggests that the species colonized these areas only after the ice melted. In addition, the observation of a single haplotype strongly suggests that the subantarctic colonization is sufficiently recent that no new mutations have appeared in any of these regions. The large-scale spread of genetic variants has been observed during the recolonization of newly available empty habitats for both buoyant (D. antarctica, Fraser et al. 2010a; M. pyrifera, Alberto et al. 2010, 2011) and non-buoyant seaweeds (M. laminarioides, Faugeron et al. 2001; G. skottsbergii, Faugeron et al. 2004). During spatial expansion, gene surfing effects may contribute to the reduction of diversity in the recolonized region (Klopfstein et al. 2006; Hallatschek et al. 2007; Excoffier and Ray 2008; also see chapter by Neiva et al. (2016) in this volume). Indeed, gene surfing could lead to the presence of one or a few haplotypes over large recently colonized geographic areas (Klopfstein et al. 2006; Hallatschek et al. 2007; Excoffier and Ray 2008; Neiva et al. 2010). And finally, after the colonization of the region affected by ice, a density-blocking effect could have limited the establishment of new haplotypes allowing for the persistence of founder effect signatures long after spatial expansion is completed (De Meester et al. 2002; Waters et al. 2013). A better sampling coverage of the Magellan province and more polymorphic markers would be necessary to specifically test these various hypotheses.

Interestingly, there are two different hypothesized source populations for these post-glacial demographic expansions. One seems to be local, on the South American continent. In both M. laminarioides “south” and G. skottsbergii, population expansion apparently started from a single South American refuge. This conclusion is supported by the existence of a single central haplotype, shared by all populations, in the star-like networks of these two taxa (Fig. 10.2, Montecinos et al. 2012; Billard et al. 2015). Whereas it seems reasonable to think that the refugium was north of 42°S for M. laminarioides where most of the haplotype diversity is present, it is difficult to propose an exact location for the refuge of G.skottsbergii. For G. skottsbergii, the same central haplotype was found near the 42°S range limit, on the Southern tip of South America, and on the Falkland Islands, and no clear difference in haplotype diversity was observed over the whole species distribution range (41°–55°S). On the other hand, the source population of D. antarctica “subantarctic” for the post-glacial expansion in Chile was located in the New Zealand Subantarctic Islands (Fraser et al. 2009, 2010a, b). A similar scenario of recent transoceanic dispersal from New Zealand can also be inferred from the genetic diversity of the red alga Gracilaria chilensis (Guillemin et al. 2014). For ITS2, the only shared haplotype between both sides of the Pacific Ocean for G.chilensis was the central haplotype in the star-like network in Chile. This gives evidence for a recent population expansion after a founder effect due to the migration to Chile from New Zealand (Guillemin et al. 2014). One other seaweed shares its single Patagonian haplotype with subantarctic islands (South Georgia, Marion and Macquire), the giant kelp M. pyrifera (Macaya and Zuccarello 2010a, b). Because little diversity was found in mitochondrial sequences of M. pyrifera, it is difficult to infer the original source population of this subantarctic demographic expansion based on mtDNA phylogeography alone. Other genetic markers are required to make further inferences. Further discussion of trans-Pacific connectivity can be found in Chapter by Fraser (2016 in this volume). Moreover, more species should be studied to understand the history of the Magellan Province, which hosts high species richness despite the regular perturbations by glacial cycles.

10.6 Prospects and Challenges Ahead

Most seaweed phylogeographic studies show that the SEP coast houses a rich cryptic diversity. Of the 12 studies listed in Table 10.1, six have revealed the existence of crypticspecies or subspecies: in Lessonia (Tellier et al. 2009), Durvillaea (Fraser et al. 2009, 2010a, b), Adenocystis (Fraser et al. 2013), Mazzaella (Montecinos et al. 2012) and Nothogenia (Lindstrom et al. 2015). These results suggest that species diversity is underestimated in the region (see Peters et al. 2010; Fraser et al. 2013). Because the existence of high cryptic diversity could obscure biogeographic patterns (Riddle and Hafner 1999), future phylogeographic studies may lead to new biogeographic paradigms (for an example see the case of the Canadian Arctic marine flora in Saunders and McDevit 2013 where molecular data have allowed the authors to revisit hypotheses about the evolutionary origins and migration of algal taxa in this region). However, strong patterns have emerged from this first comparative study. First, different studies suggest parapatric and/or peripatric speciation occurs along the linear coast of SEP. Some speciation events seem to have taken place at the limit of the Intermediate Area and the Peruvian province (30–33°S). Yet other events of divergence do not correspond with any biogeographic limit or clear ecological barriers to gene flow. In this last case, the role of stochasticity associated with climatic and tectonic catastrophes needs to be further explored as a source of phylogeographic discontinuity. Moreover, in some morphospecies the location of phylogeographic discontinuities have not been clearly pinpointed due to logistical difficulties in accessing sites, which lead to large gaps in sampling. These gaps are most apparent in the Magellan province (between 44°S and 52°S, where access to the benthic habitat is impossible from land and very difficult by boat) and in the Peruvian province (i.e. between 18°S and 24°S, a region where few roads give access to the coast). Access to samples from these areas is essential to better assess species diversity along the SEP and test speciation or recolonization scenarios. Second, if population turnover is indeed high enough to promote genetic differentiation through founder and monopolization effects, effective dispersal is expected to be low. Dispersal and gene flow should be assessed at appropriate spatial scales to test this hypothesis. In the case of strong reductions in gene flow, even slight environmental differences may allow directional selection to promote local adaptation. This is an interesting perspective that future phylogeographic studies could include either through eco-physiological experimentation or by combining analyses of both neutral and selected markers using NGS technology and population genomics approaches (Beaumont and Balding 2004; Luikart et al. 2003). Third, several (cryptic) species actually colonized the SEP from New Zealand soon after the LGM. In this context, it could be interesting to investigate whether species diversity present along the SEP is the result of elevated local speciation rates (Center of Origin hypothesis) or rather due to the accumulation of species formed elsewhere (Center of Accumulation hypothesis; Briggs 2000; Barber 2009).

From a more applied point of view, these new phylogeographic results should lead to changes in management strategies and conservation of natural resources. Small fishing villages along the SEP sometimes heavily rely on algal communities as economically important resources. Both red (G. chilensis, Chondracanthus chamissoi, Pyropia spp., Sarcothalia crispata, M. laminarioidesand G. skottsbergii) and brown (Lessonia spp., D. antarctica and M. pyrifera) seaweeds are harvested along the coast (Buschmann et al. 2001; Guillemin et al. 2008; Vásquez 2008; Tellier et al. 2011b). Morpho-species with crypticdiversity should be taken into account when conservation and/or management programs are developed (Tellier et al. 2011b) if differences in population demographics or ecological niches lead to differing susceptibility to environmental threats. For example, ecological differences between L.berteroana and L. spicata in temperature and desiccation sensitivity (Oppliger et al. 2011, 2012; López-Cristoffanini et al. 2013) suggest that the species will experience different susceptibilities to events like ENSO. Finally, several species of algae are cultivated in Chile. Breeding strategies are emerging (Buschmann et al. 2014) and might face difficulties if reproductive barriers exist between cryptic species. Such reproductive isolation exists between L. spicata and L. berteroana in their overlapping distribution ranges (Tellier et al. 2011a). Taking into account the complex evolutionary processes occurring at large spatial and temporal scales is a necessity for these applied issues, and offers interesting perspectives of interactions among multiple research lines and disciplines.



This research was supported by CONICYT FONDECYT/REGULAR No. 1130797 and Centro FONDAP IDEAL No. 15150003 to MLG and FONDECYT/INICIACION No. 11121504 to FT. Additional support came from CONICYT PCCI/Proyectos de Intercambio No. PCCI130047, The Nucleo Milenio “Centro de Conservación Marina”—RC130004, the French Research Agency ANR-ECOKELP (ANR 06 BDIV 012) and International Research Network ‘‘Diversity, Evolution and Biotechnology of Marine Algae’’ (GDRI No. 0803).


  1. Alberto F, Raimondi PT, Reed DC, Coelho NC, Leblois R, Whitmer A, Serräo EA. Habitat continuity and geographic distance predict population genetic differentiation in giant kelp. Ecology. 2010;91:49–56.PubMedCrossRefGoogle Scholar
  2. Alberto F, Raimondi PT, Reed DC, Watson JR, Siegel DA, Mitarai S, Coelho NC, Serräo EA. Isolation by oceanographic distance explains genetic structure for Macrocystis pyrifera in the Santa Barbara Channel. Mol Ecol. 2011;20:2543–54.PubMedCrossRefGoogle Scholar
  3. Anacker BL, Strauss SY. The geography and ecology of plant speciation: range overlap and niche divergence in sister species. Proc R Soc B. 2014;281:20132980.PubMedCentralPubMedCrossRefGoogle Scholar
  4. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Ann Rev Ecol Sys. 1987;18:489–522.CrossRefGoogle Scholar
  5. Baldwin BG. Origin of the serpentine-endemic herb Layia discoidea from the widespread L. glandulosa (Compositae). Evolution. 2005;59(11):2473–9.PubMedGoogle Scholar
  6. Barber PH. The challenge of understanding the Coral Triangle biodiversity hotspot. J Biogeogr. 2009;36:1845–6.CrossRefGoogle Scholar
  7. Beaumont MA, Balding DJ. Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol. 2004;13:969–80.PubMedCrossRefGoogle Scholar
  8. Belkin IM, Gordon AL. Southern Ocean fronts from the Greenwich meridian to Tasmania. J Geophys Res. 1996;101(C2):3675–96.CrossRefGoogle Scholar
  9. Billard E, Reyes J, Mansilla A, Faugeron S, Guillemin ML. Deep genetic divergence between austral populations of the red alga Gigartina skottsbergii reveals a cryptic species endemic to the Antarctic continent. Pol Biol. 2015;. doi:10.1007/s00300-015-1762-4.Google Scholar
  10. Boo GH, Mansilla A, Nelson W, Bellgrove A, Boo SM. Genetic connectivity between trans-oceanic populations of Capreolia implexa (Gelidiales, Rhodophyta) in cool temperate waters of Australasia and Chile. Aquat Bot. 2014;119:73–9.CrossRefGoogle Scholar
  11. Brante A, Fernández M, Viard F. Phylogeography and biogeography concordance in the marine gastropod Crepipatella dilatata (Calyptraeidae) along the southeastern Pacific coast. J Hered. 2012;103(5):630–7.PubMedCrossRefGoogle Scholar
  12. Brattström H, Johanssen A. Ecological and regional zoogeography of the marine benthic fauna of Chile. Sarsia. 1983;68:289–339.Google Scholar
  13. Briggs JC. Centrifugal speciation and centres of origin. J Biogeogr. 2000;27:1183–8.CrossRefGoogle Scholar
  14. Broitman BR, Navarrete SA, Smith F, Gaines SD. Geographic variation of southeastern Pacific intertidal communities. Mar Ecol Prog Ser. 2001;224:21–34.CrossRefGoogle Scholar
  15. Buschmann AH, Correa JA, Westermeier R, Hernández-González MC, Norambuena R. Red algal farming in Chile: a review. Aquaculture. 2001;194:203–20.CrossRefGoogle Scholar
  16. Buschmann AH, Prescott S, Potin P, Faugeron S, Vasquez JA, Camus C, Infante J, Hernández-González MC, Gutierrez A, Varela DA. The status of kelp exploitation and marine agronomy, with emphasis on Macrocystis pyrifera, in Chile. Adv Bot Res. 2014;71:161–88.CrossRefGoogle Scholar
  17. Camus PA. Procesos regionales y fitogeografía en el Pacífico Suroriental: el efecto de ‘El Niño-Oscilación del Sur’. Rev Chil Hist Nat. 1990;63:11–7.Google Scholar
  18. Camus PA. Biogeografía marina de Chile continental. Rev Chil Hist Nat. 2001;74(3):587–617.CrossRefGoogle Scholar
  19. Cárdenas L, Castilla JC, Viard F. A phylogeographical analysis across three biogeographical provinces of the south-eastern Pacific: the case of the marine gastropod Concholepas concholepas. J Biogeogr. 2009;36:969–81.CrossRefGoogle Scholar
  20. Castilla JC. Earthquake-caused coastal uplift and its effects on rocky intertidal kelp communities. Science. 1988;242(4877):440–3.PubMedCrossRefGoogle Scholar
  21. Castilla JC, Manriquez PH, Camaño A. Effects of rocky shore coseismic uplift and the 2010 Chilean mega-earthquake on intertidal biomarker species. Mar Ecol Prog Ser. 2010;418:17–23.CrossRefGoogle Scholar
  22. Crawford DJ. Progenitor-derivative species pairs and plant speciation. Taxon. 2010;59(5):1413–23.Google Scholar
  23. Crawford DJ, Landolt E, Les DH, Kimball RT. Speciation in duckweeds (Lemnaceae): phylogenetic and ecological inferences. Aliso. 2006;22(1):229–40.Google Scholar
  24. Darwin C. Voyages of the adventure and Beagle, vol. III. London: H. Colburn; 1839. p. 617.Google Scholar
  25. De Meester L, Gómez A, Okamura B, Schwenk K. The Monopolization Hypothesis and the dispersal–gene flow paradox in aquatic organisms. Acta Oecol. 2002;23:121–35.CrossRefGoogle Scholar
  26. Durrant HMS, Burridge CP, Kelaher BP, Barrett NS, Edgar GJ, Coleman MA. Implications of macroalgal isolation by distance for networks of marine protected areas. Cons Biol. 2014;28(2):438–45.CrossRefGoogle Scholar
  27. Excoffier E, Ray N. Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol. 2008;23(7):347–51.PubMedCrossRefGoogle Scholar
  28. Faugeron S, Valero M, Destombe C, Martínez EA, Correa JA. Hierarchical spatial structure and discriminant analysis of genetic diversity in the red alga Mazzaella laminarioides (Gigartinales, Rhodophyta). J Phycol. 2001;37:705–16.CrossRefGoogle Scholar
  29. Faugeron S, Martínez EA, Correa JA, Cardenas L, Destombe C, Valero M. Reduced genetic diversity and increased population differentiation in peripheral and over-harvested populations of Gigartina skottsbergii (Rhodophyta, Gigartinales) in southern Chile. J Phycol. 2004;40:454–62.CrossRefGoogle Scholar
  30. Faugeron S, Martínez EA, Correa JA, Billot C. Long-term copper mine waste disposal in northern Chile associated with gene flow disruption of the intertidal Lessonia nigrescens. Mar Ecol Prog Ser. 2005;288:129–40.CrossRefGoogle Scholar
  31. Fenberg PB, Menge BA, Raimondi PT, Rivadeneira MM. Biogeographic structure of the northeastern Pacific rocky intertidal: the role of upwelling and dispersal to drive patterns. Ecography. 2015;38(1):83–95.CrossRefGoogle Scholar
  32. Fernández M, Jaramillo E, Marquet PA, Moreno CA, Navarrete SA, Ojeda FP, Valdovinos CR, Vasquez JA. Diversity, dynamics and biogeography of Chilean benthic nearshore ecosystems: an overview and guidelines for conservation. Rev Chil Hist Nat. 2000;73:797–830.CrossRefGoogle Scholar
  33. Fraser CI. Change in Southern Hemisphere intertidal communities through climate cycles: the role of dispersing algae. In: Hu ZM, Fraser CI, editors. Seaweed phylogeography: adaptation and evolution of seaweeds under environmental change. Berlin: Springer; 2016.Google Scholar
  34. Fraser CI, Nikula R, Spencer HG, Waters JM. Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proc Nat Acad Sci USA. 2009;106:3249–53.PubMedCentralPubMedCrossRefGoogle Scholar
  35. Fraser CI, Thiel M, Spencer HG, Wasters JM. Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp. BMC Evol Biol. 2010a;10:203.PubMedCentralPubMedCrossRefGoogle Scholar
  36. Fraser CI, Winter DJ, Spencer HG, Waters JM. Multigene phylogeny of the southern bull-kelp genus Durvillaea (Phaeophyceae: Fucales). Mol Phylogenet Evol. 2010b;57:1301–11.PubMedCrossRefGoogle Scholar
  37. Fraser CI, Zuccarello GC, Spencer HG, Salvatore LC, Garcia GR, Waters JM. Genetic affinities between trans-oceanic populations of non-buoyant macroalgae in the high latitudes of the Southern Hemisphere. PLoS ONE. 2013;8(7):e69138.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Fuentes K, Brante A. Megadisturbances and ecological recovery in the intertidal zone: the role of interspecific competition between bioengineer mussel species. Mar Ecol Prog Ser. 2014;515:161–72.CrossRefGoogle Scholar
  39. Funk DJ, Omland KE. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Ann Rev Ecol Evol Syst. 2003;34:397–423.CrossRefGoogle Scholar
  40. González A, Beltrán J, Hiriart-Bertrand L, Flores V, de Reviers B, Correa JA, Santelices B. Identification of cryptic species in the Lessonia nigrescens complex (Phaeophyceae, Laminariales). J Phycol. 2012;48:1153–65.CrossRefGoogle Scholar
  41. González-Wevar CA, Hüne M, Cañete JI, Mansilla A, Nakano T, Poulin E. Towards a model of postglacial biogeography in shallow marine species along the Patagonian Province: lessons from the limpet Nacella magellanica (Gmelin, 1791). BMC Evol Biol. 2012;12:139.PubMedCentralPubMedCrossRefGoogle Scholar
  42. Gottlieb LD. Rethinking classic examples of recent speciation in plants. New Phytol. 2004;161:71–82.CrossRefGoogle Scholar
  43. Grossenbacher DL, Veloz SD, Sexton JP. Niche and range size patterns suggest that speciation begins in small, ecologically diverged populations in North American monkeyflowers (Mimulus spp.). Evolution. 2014;68:1270–80.PubMedCrossRefGoogle Scholar
  44. Guillemin M-L, Faugeron S, Destombe C, Viard F, Correa JA, Valero M. Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: how farming practices favor asexual reproduction and heterozygosity. Evolution. 2008;62:1500–19.PubMedCrossRefGoogle Scholar
  45. Guillemin M-L, Valero M, Faugeron S, Nelson W, Destombe C. Tracing the trans-Pacific evolutionary history of a domesticated seaweed (Gracilaria chilensis) with archaeological and genetic data. PLoS ONE. 2014;9(12):e114039.PubMedCentralPubMedCrossRefGoogle Scholar
  46. Hallatschek O, Hersen P, Ramanathan S, Nelson DR. Genetic drift at expanding frontiers promotes gene segregation. Proc Nat Acad Sci USA. 2007;104(50):19926–30.PubMedCentralPubMedCrossRefGoogle Scholar
  47. Haye PA, Muñoz-Herrera NC. Isolation with differentiation followed by expansion with admixture in the tunicate Pyura chilensis. BMC Evol Biol. 2013;13:252.PubMedCentralPubMedCrossRefGoogle Scholar
  48. Haye PA, Salinas P, Acuña E, Poulin E. Heterochronic phenotypic plasticity with lack of genetic differentiation in the southeastern Pacific squat lobster Pleuroncodes monodon. Evol Dev. 2010;12(6):628–34.PubMedCrossRefGoogle Scholar
  49. Haye PA, Varela AI, Thiel M. Genetic signatures of rafting dispersal in algal-dwelling brooders Limnoria spp. (Isopoda) along the SE Pacific (Chile). Mar Ecol Prog Ser. 2012;455:111–22.CrossRefGoogle Scholar
  50. Haye PA, Segovia NI, Muñoz-Herrera NC, Gálvez FE, Martinez A, Meynard A, Pardo-Gandarillas MC, Poulin E, Faugeron S. Phylogeographic structure in benthic marine invertebrates of the Southeast Pacific coast of Chile with differing dispersal potential. PLoS ONE. 2014;9(2):e88613.PubMedCentralPubMedCrossRefGoogle Scholar
  51. Hernández-Miranda E, Cisterna J, Díaz-Cabrera E, Veas R, Quinones RA. Epibenthic macrofaunal community response after a mega-earthquake and tsunami in a shallow bay off central-south Chile. Mar Biol. 2014;161(3):681–96.CrossRefGoogle Scholar
  52. Hormazabal S, Shaffer G, Leth O. Coastal transitions zone off Chile. J Geophys Res. 2004;109:1–13.Google Scholar
  53. Hulton N, Sugden D, Payne A, Clapperton C. Glacier modeling and the climate of Patagonia during the last glacial maximum. Quat Res. 1994;42(1):1–19.CrossRefGoogle Scholar
  54. Hulton NRJ, Purves RS, McCulloch RD, Sugden DE, Bentley MJ. The last glacial maximum and deglaciation in southern South America. Quat Sci Rev. 2002;21:233–41.CrossRefGoogle Scholar
  55. Jaramillo E, Dugan JE, Hubbard DM, Melnick D, Manzano M, Duarte C, Campos C, Sanchez R. Ecological implications of extreme events: footprints of the 2010 earthquake along the Chilean coast. PLoS ONE. 2012;7(5):e35348.PubMedCentralPubMedCrossRefGoogle Scholar
  56. Kaiser J, Lamy F, Hebbeln D. A 70-kyr sea surface temperature record off southern Chile (Ocean Drilling Program Site 1233). Paleoceanography. 2005;20:PA4009.CrossRefGoogle Scholar
  57. Keith SA, Kerswell AP, Connolly SR. Global diversity of marine macroalgae: environmental conditions explain less variation in the tropics. Gobal Ecol Biogeogr. 2014;23:517–29.CrossRefGoogle Scholar
  58. Kerswell AP. Global biodiversity patterns of benthic marine algae. Ecology. 2006;87:2479–88.PubMedCrossRefGoogle Scholar
  59. Kinlan BP, Gaines SD. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology. 2003;84(8):2007–20.CrossRefGoogle Scholar
  60. Klopfstein S, Currat M, Excoffier L. The fate of mutations surfing on the wave of a range expansion. Mol Biol Evol. 2006;23(3):482–90.PubMedCrossRefGoogle Scholar
  61. Knowlton N. Sibling species in the sea. Ann Rev Ecol Syst. 1993;24:189–216.CrossRefGoogle Scholar
  62. Knowlton N. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia. 2000;420(1):73–90.CrossRefGoogle Scholar
  63. Koch K, Thiel M, Tellier F, Hagen W, Graeve M, Tala F, Laeseke P, Bischof K. Species separation within the Lessonia nigrescens complex (Phaeophyceae, Laminariales) is mirrored by ecophysiological traits. Bot Mar. 2015;58(2):81–92.Google Scholar
  64. Lachkar Z, Gruber N. A comparative study of biological production in eastern boundary upwelling systems using an artificial neural network. Biogeosciences. 2012;9(1):293–308.CrossRefGoogle Scholar
  65. Leliaert F, Verbruggen H, Vanormelingen P, Steen F, Lopez-Bautista JM, Zuccarello GC, De Clerck O. DNA-based species delimitation in algae. Eur J Phycol. 2014;49:179–96.CrossRefGoogle Scholar
  66. Lindstrom SC, Gabrielson PW, Hughey JR, Macaya EC, Nelson WA. Sequencing of historic and modern specimens reveals cryptic diversity in Nothogenia (Scinaiaceae, Rhodophyta). Phycologia. 2015;54(2):97–108.CrossRefGoogle Scholar
  67. Locarnini RA, Mishonov AV, Antonov JI, Boyer TP, Garcia HE, Branova HA, Zweng MM, Johnson DR. World Ocean Atlas 2009, vol. 1. Temperature, NOAA Atlas NESDIS. 2010, p. 68.Google Scholar
  68. López-Cristoffanini C, Tellier F, Otaíza R, Correa JA, Contreras-Porcia L. Tolerance to air exposure: a feature driving the latitudinal distribution of two sibling kelp species. Bot Mar. 2013;56(5–6):431–40.Google Scholar
  69. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet. 2003;4:981–94.PubMedCrossRefGoogle Scholar
  70. Macaya EC, Zuccarello GC. DNA barcoding and genetic divergence in the giant kelp Macrocystis (Laminariales). J Phycol. 2010a;46:736–42.CrossRefGoogle Scholar
  71. Macaya EC, Zuccarello GC. Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol Prog Ser. 2010b;420:103–12.CrossRefGoogle Scholar
  72. Macaya EC, Lopez B, Tala F, Tellier F, Thiel M. Flot and raft: role of buoyant seaweeds in the phylogeography and genetic structure of non-buoyant associated flora. In: Hu ZM, Fraser CI, editors. Seaweed phylogeography: adaptation and evolution of seaweeds under environmental change. Berlin: Springer; 2016.Google Scholar
  73. Martin P, Zuccarello GC. Molecular phylogeny and timing of radiation in Lessonia (Phaeophyceae, Laminariales). Phycol Res. 2012;60(4):276–87.CrossRefGoogle Scholar
  74. Martínez EA, Cárdenas L, Pinto R. Recovery and genetic diversity of the intertidal kelp Lessonia nigrescens (Phaeophyceae) 20 years after El Niño 1982/1983. J Phycol. 2003;39(3):504–8.CrossRefGoogle Scholar
  75. Mayr E. Change of genetic environment and evolution. In: Huxley J, Hardy AC, Ford E, editors. Evolution as a process. London: Allen and Unwin; 1954. p. 157–80.Google Scholar
  76. McCulloch RD, Bentley MJ, Purves RS, Hulton NRJ, Sugden DE, Clapperton CM. Climatic inferences from glacial and palaeoecological evidence at the last glacial termination, southern South America. J Quat Sci. 2000;15:409–17.CrossRefGoogle Scholar
  77. Meneses I, Santelices B. Patterns and breaking points in the distribution of benthic algae along the temperate Pacific coast of South America. Rev Chil Hist Nat. 2000;73(4):615–23.CrossRefGoogle Scholar
  78. Mohtadi M, Hebbeln D. Mechanisms and variations of the paleoproductivity off northern Chile (24°S–33°S) during the last 40,000 years. Paleoceanography. 2004;19:20–3.CrossRefGoogle Scholar
  79. Montecinos A, Broitman BR, Faugeron S, Haye PA, Tellier F, Guillemin ML. Species replacement along a linear coastal habitat: phylogeography and speciation in the red alga Mazzaella laminarioides along the South East Pacific. BMC Evol Biol. 2012;12(1):97.PubMedCentralPubMedCrossRefGoogle Scholar
  80. Moy CM, Seltzer GO, Rodbell DT, Anderson DM. Variability of El Niño/Southern Oscillation activity at millennial timescales during the Holocene epoch. Nature. 2002;420(6912):162–5.PubMedCrossRefGoogle Scholar
  81. Neiva J, Pearson GA, Valero M, Serräo EA. Surfing the wave on a borrowed board: range expansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L. Mol Ecol. 2010;19(21):4812–22.PubMedCrossRefGoogle Scholar
  82. Neiva J, Pearson GA, Valero M, Serrão EA. Fine-scale genetic breaks driven by historical range dynamics and ongoing density-barrier effects in the estuarine seaweed Fucus ceranoides L. BMC Evol Biol. 2012;12:78.PubMedCentralPubMedCrossRefGoogle Scholar
  83. Neiva J, Serrão EA, Assis J, Pearson GA, Coyer JA, Olsen JL, Hoarau G, Valero M. Climate oscillations, range shifts and phylogeographic patterns of North Atlantic Fucaceae. In: Hu ZM, Fraser CI, editors. Seaweed phylogeography: adaptation and evolution of seaweeds under environmental change. Berlin: Springer; 2016.Google Scholar
  84. Nelson WA. Pyropia plicata sp. nov. (Bangiales, Rhodophyta): naming a common intertidal alga from New Zealand. PhytoKeys. 2013;21:17–28.PubMedCrossRefGoogle Scholar
  85. Nuñez JJ, Wood NK, Rabanal FE, Fontanella FM, Sites JW Jr. Amphibian phylogeography in the Antipodes: Refugia and postglacial colonization explain mitochondrial haplotype distribution in the Patagonian frog Eupsophus calcaratus (Cycloramphidae). Mol Phylogenet Evol. 2011;58(2):343–52.PubMedCrossRefGoogle Scholar
  86. Oppliger VL, Correa JA, Faugeron S, Beltran J, Tellier F, Valero M, Destombe C. Sex ratio variation in the Lessonia nigrescens complex (Laminariales, Phaeophyceae): effect of latitude, temperature, and marginality. J Phycol. 2011;47(1):5–12.CrossRefGoogle Scholar
  87. Oppliger LV, Correa JA, Engelen AH, Tellier F, Vieira V, Faugeron S, Valero M, Gomez G, Destombe C. Temperature effects on gametophyte life-history traits and geographic distribution of two cryptic kelp species. PLoS ONE. 2012;7(6):e39289.PubMedCentralPubMedCrossRefGoogle Scholar
  88. Ortega KJ, Sáez CA, Macaya EC. Changes in invertebrate assemblages inhabiting Lessonia spicata (Phaeophyceae) holdfasts after the 2010 earthquake-mediated coastal uplift in Chile. Rev Biol Mar Oceanogr. 2014;49(1):129–34.CrossRefGoogle Scholar
  89. Pardo C, Lopez L, Peña V, Hernández-Kantun J, Gall LL, Bárbara I, Barreiro R. A multilocus species delimitation reveals a striking number of species of coralline algae forming maerl in the OSPAR maritime area. PLoS ONE. 2014;9(8):e104073.PubMedCentralPubMedCrossRefGoogle Scholar
  90. Payo DA, Leliaert F, Verbruggen H, D’hondt S, Calumpong HP, De Clerck O. Extensive cryptic species diversity and fine-scale endemism in the marine red alga Portieria in the Philippines. Proc R Soc B. 2013;280:20122660.PubMedCentralPubMedCrossRefGoogle Scholar
  91. Peters AF, Mann AD, Córdova CA, Brodie J, Correa JA, Schroeder DC, Cock JM. Genetic diversity of Ectocarpus (Ectocarpales, Phaeophyceae) in Peru and northern Chile, the area of origin of the genome-sequenced strain. New Phytol. 2010;188:30–41.PubMedCrossRefGoogle Scholar
  92. Ponce JF, Rabassa J, Coronato A, Borromei AM. Palaeogeographical evolution of the Atlantic coast of Pampa and Patagonia from the last glacial maximum to the Middle Holocene. Biol J Linn Soc. 2011;103(2):363–79.CrossRefGoogle Scholar
  93. Pyron RA, Burbrink FT. Can the tropical conservatism hypothesis explain temperate species richness patterns? An inverse latitudinal biodiversity gradient in the NewWorld snake tribe Lampropeltini. Global Ecol Biogeogr. 2009;18:406–15.CrossRefGoogle Scholar
  94. Ramírez ME. Flora marina bentónica de la región Austral de Sudamérica y la Antártica. Anales Instituto Patagonia. 2010;38:57–71.Google Scholar
  95. Ramírez ME, Contreras-Porcia L, Guillemin ML, Brodie J, Valdivia C, Flores-Molina MR, Nunez A, Contador CB, Lovazzano C. Pyropia orbicularis sp. nov. (Rhodophyta, Bangiaceae) based on a population previously known as Porphyra columbina from the central coast of Chile. Phytotaxa. 2014;158(2):133–53.CrossRefGoogle Scholar
  96. Riddle BR, Hafner DJ. Species as units of analysis in ecology and biogeography: time to take the blinders off. Global Ecol Biogeogr. 1999;8(6):433–41.CrossRefGoogle Scholar
  97. Ruzzante DE, Walde SJ, Gosse JC, Cussac VE, Habit E, Zemlak TS, Adams EDM. Climate control on ancestral population dynamics: insight from Patagonian fish phylogeography. Mol Ecol. 2008;17:2234–44.PubMedCrossRefGoogle Scholar
  98. Sánchez R, Sepúlveda RD, Brante A, Cristina CTL. Spatial pattern of genetic and morphological diversity in the direct developer Acanthina monodon (Gastropoda: Mollusca). Mar Ecol Prog Ser. 2011;434:121–31.CrossRefGoogle Scholar
  99. Santelices B. Phytogeographic characterization of the temperate coast of Pacific South America. Phycologia. 1980;19(1):1–12.CrossRefGoogle Scholar
  100. Santelices B. Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr Mar Bio. 1990;128:177–276.Google Scholar
  101. Santelices B, Marquet P. Seaweeds, latitudinal diversity patterns, and Rapoport’s rule. Divers Distrib. 1998;4(2):71–5.CrossRefGoogle Scholar
  102. Santelices B, Meneses I. A reassessment of the phytogeographic characterization of temperate Pacific South America. Rev Chil Hist Nat. 2000;73:605–14.CrossRefGoogle Scholar
  103. Saunders GW, McDevit DC. DNA barcoding unmasks overlooked diversity improving knowledge on the composition and origins of the Churchill algal flora. BMC Ecol. 2013;13:9.PubMedCentralPubMedCrossRefGoogle Scholar
  104. Sérsic AN, Cosacov A, Cocucci AA, Johnson LA, Pozner R, Avila LJ, Sites JW Jr, Morando M. Emerging phylogeographical patterns of plants and terrestrial vertebrates from Patagonia. Biol J Linn Soc. 2011;103(2):475–94.CrossRefGoogle Scholar
  105. Strub PT, Mesías JM, Montecino V, Rutlant J, Salinas S. Coastal ocean circulation off western South America. In: Brink KH, Robinson AR, editors. The global coastal ocean. New York: Wiley; 1998. p. 273–313.Google Scholar
  106. Tapia FJ, Largier JL, Castillo M, Wieters EA, Navarrete SA. Latitudinal discontinuity in thermal conditions along the nearshore of Central-Northern Chile. PLoS ONE. 2014;9(10):e110841.PubMedCentralPubMedCrossRefGoogle Scholar
  107. Tarazona J, Arntz W. The Peruvian coastal upwelling system. In: Seeliger U, Kjerfve B, editors. Coastal marine ecosystems of Latin America. Ecological studies, vol. 144. Berlin: Springer; 2001. p. 229–44.CrossRefGoogle Scholar
  108. Tellier F, Meynard AP, Correa JA, Faugeron S, Valero M. Phylogeographic analyses of the 30°S south-east Pacific biogeographic transition zone establish the occurrence of a sharp genetic discontinuity in the kelp Lessonia nigrescens: Vicariance or parapatry? Mol Phylogenet Evol. 2009;53(3):679–93.PubMedCrossRefGoogle Scholar
  109. Tellier F, Tapia J, Faugeron S, Destombe C, Valero M. The Lessonia nigrescens complex (Laminariales, Phaeophyceae) shows strict parapatry and complete reproductive isolation in a secondary contact zone. J Phycol. 2011a;47:894–903.CrossRefGoogle Scholar
  110. Tellier F, Vega JMA, Broitman BR, Vasquez JA, Valero M, Faugeron S. The importance of having two species instead of one in kelp management: the Lessonia nigrescens species complex. Cah Biol Mar. 2011b;52:455–65.Google Scholar
  111. Thiel M, Macaya EC, Acuña E, Arntz WE, Bastias H, Brokordt K, Camus P, Castilla JC, Castro L, Cortes M, Dumont CP, Escribano R, Fernandez M, Gajardo JA, Gaymer CF, Gomez I, Gonzalez AE, Gonzalez HE, Haye PA, Illanes JE, Iriarte JL, Lancellotti DA, Luna-Jorquera G, Luxoro C, Manriquez PH, Marin V, Munoz P, Navarrete SA, Perez E, Poulin E, Sellanes J, Hito Sepulveda H, Stotz W, Tala F, Thomas A, Vargas C, Vasquez JA, Vega JMA. The Humboldt Current System of Northern and Central Chile: oceanographic processes, ecological interactions and socioeconomic feedback. Oceanogr Mar Biol. 2007;45:195–344.Google Scholar
  112. Tronholm A, Leliaert F, Sansón M, Afonso-Carrillo J, Tyberghein L, Verbruggen H, De Clerk O. Contrasting geographical distributions as a result of thermal tolerance and long-distance dispersal in two allegedly widespread tropical brown algae. PLoS ONE. 2012;7:e30813.PubMedCentralPubMedCrossRefGoogle Scholar
  113. Valero M, Destombe C, Mauger S, Ribout C, Engel CR, Daguin-Thiebaut C, Tellier F. Using genetic tools for sustainable management of kelps: a literature review and the example of Laminaria digitata. Cah Biol Mar. 2011;52(4):467–83.Google Scholar
  114. Varela AI, Haye PA. The marine brooder Excirolana braziliensis (Crustacea: Isopoda) is also a complex of cryptic species on the coast of Chile. Rev Chil Hist Nat. 2012;85:495–502.CrossRefGoogle Scholar
  115. Vasquez. Production, use and fate of Chilean brown seaweeds: re-sources for a sustainable fishery. J App Phycol. 2008;20:457–67.CrossRefGoogle Scholar
  116. Verleye TJ, Louwye S. Late Quaternary environmental changes and latitudinal shifts of the Antarctic Circumpolar Current as recorded by dinoflagellate cysts from offshore Chile (41°S). Quat Sci Rev. 2010;29(7):1025–39.CrossRefGoogle Scholar
  117. Vianna JA, Medina-Vogel G, Chehébar C, Sielfeld W, Olavarria C, Faugeron S. Phylogeography of the Patagonian otter Lontra provocax: adaptive divergence to marine habitat or signature of southern glacial refugia? BMC Evol Biol. 2011;11:53.PubMedCentralPubMedCrossRefGoogle Scholar
  118. Vidal R, Meneses I, Smith M. Phylogeography of the genus Spongites (Corallinales, Rhodophyta) from Chile. J Phycol. 2008;44:173–82.CrossRefGoogle Scholar
  119. Vieira C, D’hondt S, De Clerck O, Payri CE. Toward an inordinate fondness for stars, beetles and Lobophora? Species diversity of the genus Lobophora (Dictyotales, Phaeophyceae) in New Caledonia. J Phycol. 2014;50(6):1101–19.CrossRefGoogle Scholar
  120. Vieira VM, Oppliger LV, Engelen AH, Correa JA. A new method to quantify and compare the multiple components of fitness—A study case with Kelp niche partition by divergent microstage adaptations to temperature. PLoS ONE. 2015;10(3):e0119670.PubMedCentralPubMedCrossRefGoogle Scholar
  121. Walser B, Haag CR. Strong intraspecific variation in genetic diversity and genetic differentiation in Daphnia magna: the effects of population turnover and population size. Mol Ecol. 2012;21:851–61.PubMedCrossRefGoogle Scholar
  122. Waters JM, Fraser CI, Hewitt GM. Founder takes all: density-dependent processes structure biodiversity. Trends Ecol Evol. 2013;28(2):78–85.PubMedCrossRefGoogle Scholar
  123. Weinberger F, Guillemin M-L, Destombe C, Valero M, Faugeron S, Correa JA, Pohnert G, Pehlke C, Kloareg B, Potin P. Defense evolution in the Gracilariaceae (Rhodophyta): substrate-regulated oxidation of agar oligosaccharides is more ancient than the oligoagar-activated oxidative burst. J Phycol. 2010;46(5):958–68.CrossRefGoogle Scholar
  124. Xu J, Pérez-Losada M, Jara CG, Crandall KA. Pleistocene glaciation leaves deep signature on the freshwater crab Aegla alacalufi in Chilean Patagonia. Mol Ecol. 2009;18:904–18.PubMedCrossRefGoogle Scholar
  125. Zakas C, Binford J, Navarrete SA, Wares JP. Restricted gene flow in Chilean barnacles reflects an oceanographic and biogeographic transition zone. Mar Ecol Prog Ser. 2009;394:165–77.CrossRefGoogle Scholar
  126. Zemlak TS, Habit EM, Walde SJ, Carrea C, Ruzzante DE. Surviving historical Patagonian landscapes and climate: molecular insights from Galaxias maculatus. BMC Evol Biol. 2010;10:67.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Marie-Laure Guillemin
    • 1
    • 2
  • Myriam Valero
    • 2
  • Florence Tellier
    • 3
  • Erasmo C. Macaya
    • 4
    • 5
  • Christophe Destombe
    • 2
  • Sylvain Faugeron
    • 2
    • 6
  1. 1.Instituto de Ciencias Ambientales y Evolutivas, Facultad de CienciasUniversidad Austral de ChileValdiviaChile
  2. 2.CNRS, Sorbonne UniversitésUPMC University Paris VI, UMI 3614, Evolutionary Biology and Ecology of Algae, Station Biologique de RoscoffRoscoffFrance
  3. 3.Departamento de Ecología, Facultad de CienciasUniversidad Católica de la Santísima ConcepciónConcepciónChile
  4. 4.Laboratorio de Estudios Algales (ALGALAB), Departamento de OceanografíaUniversidad de ConcepciónConcepciónChile
  5. 5.Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI)CoquimboChile
  6. 6.Centro de Conservación Marina and CeBiB, Facultad de Ciencias BiológicasPontificia Universidad Católica de ChileSantiagoChile

Personalised recommendations