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Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times

K. Elmer,Topi K. Lehtonen,Andreas F. Kautt,C. Harrod,A. Meyer

Published 2012 in BMC Biology

ABSTRACT

Background: After a volcano erupts, a lake may form in the cooled crater and become an isolated aquatic ecosystem. This makes fishes in crater lakes informative for understanding sympatric evolution and ecological diversification in barren environments. From a geological and limnological perspective, such research offers insight about the process of crater lake ecosystem establishment and speciation. In the present study we use genetic and coalescence approaches to infer the colonization history of Midas cichlid fishes (Amphilophus cf. citrinellus) that inhabit a very young crater lake in Nicaragua-the ca. 1800 year-old Lake Apoyeque. This lake holds two sympatric, endemic morphs of Midas cichlid: one with large, hypertrophied lips (~20% of the total population) and another with thin lips. Here we test the associated ecological, morphological and genetic diversification of these two morphs and their potential to represent incipient speciation. Results: Gene coalescence analyses [11 microsatellite loci and mitochondrial DNA (mtDNA) sequences] suggest that crater lake Apoyeque was colonized in a single event from the large neighbouring great lake Managua only about 100 years ago. This founding in historic times is also reflected in the extremely low nuclear and mitochondrial genetic diversity in Apoyeque. We found that sympatric adult thinand thick-lipped fishes occupy distinct ecological trophic niches. Diet, body shape, head width, pharyngeal jaw size and shape and stable isotope values all differ significantly between the two lip-morphs. The eco-morphological features pharyngeal jaw shape, body shape, stomach contents and stable isotopes (δ15N) all show a bimodal distribution of traits, which is compatible with the expectations of an initial stage of ecological speciation under disruptive selection. Genetic differentiation between the thinand thicklipped population is weak at mtDNA sequence (FST = 0.018) and absent at nuclear microsatellite loci (FST < 0.001). Conclusions: This study provides empirical evidence of eco-morphological differentiation occurring very quickly after the colonization of a new and vacant habitat. Exceptionally low levels of neutral genetic diversity and inference from coalescence indicates that the Midas cichlid population in Apoyeque is much younger (ca. 100 years or generations old) than the crater itself (ca. 1 800 years old). This suggests either that the crater remained empty for many hundreds of years after its formation or that remnant volcanic activity prevented the establishment of a stable fish population during the early life of the crater lake. Based on our findings of eco-morphological variation in the Apoyeque Midas cichlids, and known patterns of adaptation in Midas cichlids in general, we suggest that this population may be in a very early stage of speciation (incipient species), promoted by disruptive selection and ecological diversification. Background Since Darwin and Wallace, the study of island inhabitants has greatly influenced evolutionary and ecological research [1]. In many respects, crater lakes are the aquatic equivalent to islands. Like islands, the small size, distinct boundaries, simplified biota, young age, geographical isolation and frequently well-known geological history of crater lakes makes them well-suited to study the diversification of sister taxa [1-3]. The physical isolation of crater lakes means that after the first seeding by a colonizing lineage evolution may proceed rapidly in situ. Indeed, crater lakes have provided the most compelling examples of sympatric ecological speciation of fishes, particularly cichlid fishes [4-7]. Intralacustrine speciation in depauperate habitats (for example, postglacial lakes and crater lakes) typically proceeds due to disruptive ecological * Correspondence: axel.meyer@uni-konstanz.de 1 Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457 Konstanz, Germany Full list of author information is available at the end of the article BioMed Central © 2010 Elmer et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Elmer et al. BMC Biology 2010, 8:60 http://www.biomedcentral.com/1741-7007/8/60 Page 2 of 15 selection [8], though the rapidity, strength and completeness of this process depends on a number of population and environmental factors [5,9-11]. Well-known examples of this phenomenon include the benthic and planktivorous populations of sticklebacks [12,13], introduced salmon populations [14] and whitefish [15,16] in isolated lakes. Cichlid fishes are pre-eminent non-model organisms for the study of ecological speciation because of their trophic polymorphism and rapid evolution [17,18]. Mesoamerican fishes of the Midas cichlid species complex (the Amphilophus citrinellus species group) are particularly variable in trophic characteristics such as body shape and pharyngeal jaw morphology, as well as maintaining a striking colour polymorphism [19-21] (for a review of the crater lakes and species complex see [22]). One of the most renowned examples of ecological differentiation in the species complex is the elongate, openwater species Amphilophus zaliosus, which evolved from a high-bodied benthic ancestor by sympatric speciation within Nicaragua's oldest crater lake, Lake Apoyo [4,20]. A similarly elongate but evolutionarily independent endemic species is also found in crater lake Xiloá [22-25]. An additional trophic polymorphism of Midas cichlids is fleshy, hypertrophied lips, which is believed to be involved in harvesting invertebrates from between cracks and recesses [20]. This character is absent from most crater lake Midas cichlid populations [20,22,26] and is best known from Amphilophus labiatus, a species that occurs in the two largest and shallowest lakes in the region, the great lakes Managua and Nicaragua [20]. Apoyeque is the only crater lake that harbours a sizeable population of Midas cichlids with hypertrophied lips; the origin and diversity of this population is the focus of our current study. Western Nicaragua is underlain by an extremely active volcanism that has resulted in at least eight crater lakes that exist today (reviewed in [22]). One of the youngest of these is Apoyeque (Figure 1). The volcano last erupted only about 1800 years ago [27] and then filled with groundand rainwater to become a crater lake. The lake is small (2.5 km2) yet deep (110 m) [28,29] and, because of its steep cone shape, has a fairly small littoral zone (0.9 km2) [30]. 'Apoyeque' means 'salty water' in the regional Náhuatl language and the lake is so-named because of its high mineral content [31]. Located on the Chiltepe Peninsula, Apoyeque lies next to crater lake Xiloá and great lake Managua and yet its high crater walls (400 m) and lack of water connection make it completely aquatically isolated. Despite the crater lake Apoyeque's young age and isolation, it is home to an abundant population of Midas cichlids (Amphilophus cf. citrinellus). There are two phenotypes living in the lake: one with normal citrinellus thin lips ('thin-lipped') and one with pronounced fleshy, or hypertrophied, lips ('thick-lipped'; Figure 1). The lake is otherwise depauperate in species, only housing some small live-bearing fishes (Family Poeciliidae) and, less abundantly, the predatory cichlid Parachromis managuense [30]. In the present study, we test whether the two phenotypes (morphs) of Midas cichlid in Apoyeque originated by sympatric differentiation promoted by ecological divergence. Given the intralacustrine diversification of Midas cichlids in other crater lakes, we hypothesize that this trait of thinor thicklips may be a novel or alternative axis of ecological differentiation exploited by crater lake cichlids. First, we infer the colonization history of Figure 1 Relief map of Nicaragua showing the relevant lakes. Crater lake Apoyeque is located beside the great Lake Managua and the crater Lake Xiloá, in western Nicaragua, Central America. Two morphs of Midas cichlid are found in Apoyeque: one with fleshy lips (upper individual; 'thick-lipped') and the other with thin, normal A. citrinellus lips (lower individual; 'thin-lipped'). Elmer et al. BMC Biology 2010, 8:60 http://www.biomedcentral.com/1741-7007/8/60 Page 3 of 15 crater lake Apoyeque using population genetic and coalescent approaches, in the context of neighbouring lakes Managua and Xiloá. We specifically assess evidence for a single or multiple colonization events and see whether the age of the population corresponds to the geological age of the lake. Second, we compare ecological (diet, trophic level and pharyngeal jaw shape) and morphological (body shape, head and body size) variation between thinand thick-lipped fishes to see whether this character is associated with distinct niches, sex or maturity, or morphological difference. Third, we assess the role of disruptive natural selection in driving incipient speciation by comparing the distribution of phenotypes and genetic differentiation in Apoyeque's Midas cichlid population, with the expectation that ecological diversification should result in a bimodal distribution of ecologically relevant traits. Results Colonization and population genetics of Apoyeque and

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