Ancient Lake Titicaca (Peru/Bolivia), which is located in the northern part of the endorheic, high-elevation Altiplano (Dejoux 1994; Allmendinger et al. 1997; Pawley et al. 2001; Baker et al. 2005; Fig. 1), contains a diverse endemic fauna whose biogeographic history is poorly understood. The following two hypotheses have been proposed for the generation of endemic diversity in ancient lakes (e.g., Martens 1997). (1) These water bodies have functioned as sinks for extralimital biota over long time periods, resulting in the accumulation of phylogenetically diverse assemblages (reservoir function). (2) The lakes have served as a venue for local (intralacustrine) speciation (cradle function). Both of these contrasting scenarios assume that the paleohydrology of these lakes has played a pivotal role in the assembly of endemic biota (e.g., Martens 1997).
The history of Lake Titicaca was punctuated by a series of major hydrologic events. The lake originated during the Late Pliocene/Early Pleistocene, about 2−3 million years (My) ago (Lavenú 1992) and underwent several phases of expansion and contraction during the Late Pleistocene that were caused by glacial–interglacial cycles and associated changes in effective moisture (Wirrmann 1992; Argollo and Mourguiart 2000; Cross et al. 2000; Fritz et al. 2007; Blard et al. 2011). At least five major phases have been recognized, which are sometimes referred to as “paleolakes” (Lavenú 1981, 1995; Lavenú et al. 1984; Wirrmann 1992; Cross et al. 2000; Baker et al. 2005; also see Figs. 1C and 2).
The Mataro Lake, coeval with the Purapurani formation (Calvario/Kaluyo interglacial S5) 1.5–1.6 My ago (Lavenú 1995; also see Lavenú et al. 1984; Marshall and Sempere 1991), was 3950 m in elevation (i.e., ca. 140 m higher than at present) and constituted the largest recorded expansion of Lake Titicaca, overlapping much of the Altiplano (Fig. 1C; Lavenú et al. 1984). Lake Mataro eventually desiccated and Lake Cabana, corresponding to the Kaluyo/Sorata interglacial (S4) (Lavenú 1995; also see Lavenú et al. 1984; Marshall and Sempere 1991), developed ca. 1.1–1.0 My ago with a maximum lake-level elevation of 3900 m. The third episode gave rise to Lake Ballivián with a lake level of 3860 m (Lavenú 1981; Lavenú et al. 1984). Most authors suggest that Lake Ballivián originated during the Sorata/Choqueyapu I interglacial (S3/t3) about 0.6–0.5 My ago (Lavenú 1995; also see Lavenú et al. 1984; Marshall and Sempere 1991; but see Fornari et al. 2001).
Subsequent climatic changes resulted in the North Minchin episode, corresponding to the Choqueyapu I/II (t2) interglacial (Lavenú 1995), approximately 73–30 kiloyears (ka) ago with a lake level of 3825 m (Fornari et al. 2001), and the North Tauca episode, corresponding to the postglacial Choqueyapu II (t1) phase (Lavenú 1995), approximately 18.0–14.5 ka ago with a lake level of 3815 m (Blard et al. 2011). Lake-level fluctuations continued into the Holocene; contractions of up to 100 m depth and drastically increased salinity levels have been reported for this time interval (Betancourt et al. 2000; Cross et al. 2000). It is generally assumed that these paleohydrologic events helped shape the evolutionary history of regional aquatic biota. For example, the repeated cycles of lake extension and shrinking may have promoted dispersal and vicariance, respectively; and desiccation and associated fluctuations in salinity may have resulted in extinction (e.g., Lüssen et al. 2003; Benavides 2005).
The Lake Titicaca region contains at least 533 aquatic species (Dejoux 1994); at least 64 of these (12%) are considered to be endemic (González and Watling 2003; Lüssen et al. 2003; Benavides 2005). However, these numbers are considerably smaller than in most other ancient lake basins (e.g., Martens 1997). The relatively small number of endemic species in this lake has been attributed to (1) the possibility that the ancestral biota was tropical in origin and consequently was depleted during the uplifting of the Altiplano because few species could tolerate high elevations and/or low temperatures (de Lattin 1967); and (2) the large variation in lacustrine water chemistry during the late Cenozoic, which resulted in extinctions (Wirrmann et al. 1991; Dejoux 1994).
Despite the relatively small number of endemic species in Lake Titicaca, there are possible species flocks of pupfishes (genus Orestias; e.g., Lüssen et al. 2003), amphipods (genus Hyalella; e.g., González and Watling 2003; Väinölä 2008), and microgastropods (genus Heleobia; e.g., Hershler and Thompson 1992). The phylogenetic relationships and biogeographic history of these three groups have not been well established, although the molecular evolution of Orestias has been detailed in an unpublished dissertation (Lüssen 2003). That study included preliminary molecular-clock analyses that suggest that speciation was recent and possibly associated with Middle to Late Pleistocene paleohydrologic processes.
Virtually nothing is known about the phylogenetic relationships of the Heleobia flock (14 species) in Lake Titicaca. Altiplano congeners are mostly endemic whereas extralimital members of the genus range more widely. This prevailing biogeographical pattern suggests that Heleobia may be a particularly suitable group for investigating evolutionary diversification in the Lake Titicaca region.
We here use a molecular clock approach together with a phylogeographical analysis to address the following questions:
- 1Did Lake Titicaca serve as a biogeographic reservoir for Altiplano species or did the endemic snail lineages in the lake evolve through rapid intralacustrine speciation? This relates to the age and phylogenetic composition of the endemic fauna, and the extent to which evolutionary diversification occurred within the lake.
- 2Are diversification events in Heleobia spp. related to major paleohydrological episodes on the Altiplano? The question is associated with processes of speciation in ancient Lake Titicaca and the abiotic factors driving evolution.
- 3Are there hierarchical spatial levels of endemicity in the Lake Titicaca region? This question is related to the concept of ecological isolation of ancient lake species, that is, assumed low levels of faunal exchange between ancient lakes and their watersheds as well as between watersheds and extralimital areas.
This is the first phylogeographical study of an Altiplano invertebrate species assemblage and may contribute to a better understanding of speciation processes in Lake Titicaca. Furthermore, given that Lake Titicaca differs from most, if not all other ancient lakes in its physical and biotic features, this study may help identify the unifying patterns and processes in world-wide ancient lakes that, in general, can explain their often outstanding degree of biodiversity.