We are interested in marine ecological and evolutionary processes in the tropics and their implications in the context of global change, management and conservation. Such processes include for example dispersal, adaptation, speciation and adaptive radiation. We work mostly on reef fishes but are keen to also consider other marine organisms. Our main tool is population genomics, which we often complement with other approaches such as behavior or theory. Recent and ongoing research topics in the lab include the genomic bases of speciation and adaptive radiation, marine dispersal and gene flow, mutual mate choice, the genomic bases of color pattern in reef fishes, animal personality, mimicry or the evolution of egg trading in simultaneous hermaphrodites. Ongoing and past projects are briefly described below.
Oscar Puebla
ZMT / ICBM
Research
Ongoing projects
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Adaptive radiation, the evolutionary process whereby a lineage diversifies over a short period of time, is an important source of biological diversity. While substantial progress has been made in our understanding of the ecological contexts that provide opportunity for radiation, how this potential is realized from a genetic perspective remains largely unknown. In this project, we leverage 170 genomes to dissect the genomic architecture of adaptive radiation in the hamlets. Led by OP and Kosmas Hench in collaboration with Owen McMillan. Funded by the DFG.
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Coastal marine resources provide major ecosystem services, with about 45% of the world’s fisheries and 90% of fishing employment linked to small-scale artisanal fisheries. In the Mediterranean EU, artisanal fisheries represent 80% of fishing vessels and are estimated to provide 100,000 jobs. Yet Mediterranean marine resources are declining at an alarming rate and fishing has resulted in the overexploitation of >50% of Mediterranean fisheries resources. In this context, Marine Protected Areas (MPAs) are emerging a a key conservation and management tool. However, the Mediterranean Sea lags behind the Aichi Conservation Target 11 from the Convention on Biological Diversity (10% of sea surface protected by 2020) with only 1% of sea surface currently covered by MPAs. There is an urgent need to increase conservation efforts and improve practices that allow exploited species to persist and sustain artisanal fisheries. Yet the extent to which larvae and adults disperse outside of MPA boundaries and contribute to sustain local artisanal fisheries is still largely unknown. In order to address this question we teamed up with Stéphanie Manel and put together a EU BiodiveERsA project with partners in France, Spain and Sweden. We adopted a continuous sampling strategy along more than 1,000 km of coast in the Northwestern Mediterranean Sea to empirically scale down from regional to small-scale patterns of connectivity in four species. Led by OP, Stéphanie Manel, Katharina Fietz and Laura Benestan.
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The diversity of color patterns displayed by reef fishes is one of the most visually stunning traits in animals. While the ecological and evolutionary significance of reef fish color pattern is well documented, little is known about the genetic bases of this trait. In this project, we combine whole-genome sequencing with quantitative analysis of both color and pattern to dissect the genomic bases of this complex trait. Led by OP, Floriane Coulmance-Gayrard, Derya Akkaynak and Kosmas Hench, funded by The Future Ocean, GEOMAR and DFG.
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The attribution of the 2012 Sveriges Riksbank Prize in Economic Sciences in Memory of Alfred Nobel to the two main founders of matching theory, Lloyd Shapley and Alvin Roth, illustrates the fundamental importance and specificity of this theoretical framework. Nevertheless, matching theory has been largely underused in evolutionary biology despite the potential of this approach to address mate choice and sexual selection. The application of matching theory in evolutionary biology is more than just a theoretical curiosity; it can generate counter-intuitive predictions and lead to conclusions that differ fundamentally from classic theories. For example, it predicts that when mate choice is mutual and the stability of mating pairs is critical for successful reproduction, the evolution of assortative mating in sympatry can be a robust evolutionary outcome. In this project, we take an empirical approach to this question and analyse one year of continuous observation of mating interactions among butter hamlets with a matching perspective. Led by OP and Sophie Picq.
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Marine species tend to be characterized by wide-dispersing larvae, large population sizes, extensive geographic ranges and high fecundities. The marine environment is also more buffered than terrestrial and freshwater environments, and presents fewer barriers to the movement of organisms. These factors are thought to generally promote gene flow and thereby impede species formation. Nonetheless, the ocean harbours some of the most diverse communities on Earth. Whether and how this diversity arose in the presence of gene flow is still unresolved and poses a fantastic challenge to our understanding of the origins of biodiversity. In this project we use full-genome data to reconstruct the history of gene flow in the hamlet radiation. We are interested in particular to infer whether the hamlets diverged in full sympatry, with gene flow ongoing through the entire history of divergence, or with an initial allopatric phase followed by secondary contact. Led by OP, Cameron Walsh and Kosmas Hench.
Finalized projects
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In an influential theoretical paper, Felsenstein (1981, Evolution 35 124-138) identified recombination between loci underlying mate choice and ecological traits as a major evolutionary force acting against speciation with gene flow, with the corollary that the development of linkage disequilibrium between such loci is a fundamental step in the origin of species. Could this process take place in the absence of physical linkage? This is the question that we address in this project, using full-genome analysis and the hamlets as a model system. Led by OP and Kosmas Hench in collaboration with Owen McMillan. Funded by the DFG, Smithsonian Institute for Biodiversity Genomics and Global Genome Initiative. Link to Nature Ecology & Evolution paper here.
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Marine species tend to have extensive distributions, which are commonly attributed to the dispersal potential provided by pelagic larvae and the rarity of absolute barriers to dispersal in the ocean. Under this paradigm, the occurrence of marine microendemism without geographic isolation in species with pelagic larvae poses a dilemma. The recently described Maya hamlet (Hypoplectrus maya) is exactly such a case, being endemic to a 50-km segment of the Mesoamerican Barrier Reef System. In this project we leverage the recent development of a chromosome-resolution reference genome for Hypoplectrus to address the evolution of microendemism in the marine environment. Led by OP and Ben Moran, funded by the National Geographic Society, Northeastern University, Future Ocean Cluster of Excellence, DAAD and DFG. Link to Molecular Ecology paper here.
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Egg trading, whereby simultaneous hermaphrodites exchange each other’s eggs for fertilization, constitutes one of the few rigorously documented and most widely cited examples of direct reciprocity among unrelated individuals. Yet how egg trading may initially invade a population of non-trading simultaneous hermaphrodites is still unresolved. Here, we address this question with an analytical model that considers mate encounter rates and costs of egg production in a population that may include traders (who provide eggs for fertilization only if their partners also have eggs to reciprocate), providers (who provide eggs regardless of whether their partners have eggs to reciprocate), and withholders (“cheaters” who only mate in the male role and just use their eggs to elicit egg release from traders). Collaboration with Jorge Peña and Georg Nöldeke. Funded by The Future Ocean. Link to American Naturalist paper here.
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When there is no recombination in one sex, it is the in the heterogametic one. This observation is so consistent that it constitutes one of the few patterns that may be regarded as a ‘rule’ or a ‘law’ in biology, and Haldane proposed that it may driven by selection against recombination in the sex chromosomes. Nevertheless, differences in recombination rate between the sexes have also been reported in hermaphroditic species that lack sex chromosomes, and an alternative explanation is required in this case. In plants—the vast majority of which are hermaphroditic—selection at the haploid stage has been proposed to drive heterochiasmy. Yet few data are available for hermaphroditic animals, and barely any for hermaphroditic vertebrates. We used reciprocal crosses between two black hamlets (Hypoplectrus nigricans, Serranidae), simultaneously hermaphroditic reef fishes from the wider Caribbean, to generate high-density egg- and sperm-specific linkage maps for each parent. Link to Proceedings B publication here.
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Associations between resembling species have been noted long ago by naturalists and have been traditionally interpreted in terms of mimicry, whereby a mimetic species is naturally selected to resemble a model (Batesian and aggressive mimicry) or a co-mimic (Müllerian mimicry). Recently, it has been proposed that resemblances among reef fishes might be coincidental and that associations between them may result from social-traps, i.e. out-of-normal-context responses towards similar-looking individuals. The social-trap hypothesis is stimulating and calls for an in-depth reassessment of putative cases of mimicry in reef fishes. Nevertheless, an explicit field-based evaluation of the two hypotheses has yet to be conducted. In this project, we test five specific predictions derived from the two hypotheses in the association between the butter hamlet (Hypoplectrus unicolor, Serranidae) and the foureye butterflyfish (Chaetodon capistratus, Chaetodontidae), which was one of the associations considered to develop the social-trap hypothesis. Led by OP and Sophie Picq. Coral Reefs publication here.
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The link between ecology and reproductive isolation constitutes the cornerstone of the ecological hypothesis of speciation. Such a link can arise when traits under ecologically-based selection are also used as cues for mating (‘magic traits’), or as a byproduct of habitat choice when mating takes place within habitats. Using the butter hamlet (Hypoplectrus unicolor) as a model system , we propose that behavioral syndromes may also constitute such a link in some cases. Individuals from a natural population in Panama were tagged and their diurnal and spawning behaviors observed over two years for a total of 159 hours. Led by OP and Sophie Picq, funded by IMPRS through GEOMAR and a short-term fellowship from the Smithsonian Tropical Research Institute.
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The hamlets constitute a distinctive marine model system for the study of a variety of ecological and evolutionary processes including egg trading, sexual selection and speciation. Temporal changes in hamlet communities can potentially affect or be affected by such processes, but the dynamics of hamlet communities and their ecological drivers are still eluding ecologists. Reasons for this knowledge gap include the difficulty to identify some individuals due to extensive color pattern variation in the group, their relatively low densities and the paucity of detailed hamlet community surveys. The hamlets from La Parguera, Puerto Rico, constitute a notable exception with a thorough survey by Aguilar-Perera available for the year 2000. Seventeen years later we revisited the same reefs and conducted transect surveys covering 14,000 m2 across 16 reefs to test whether hamlet communities are temporally stable or whether temporal changes in hamlet communities may give us hints about their ecology. Link to Journal of Fish Biology publication here.
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Stocking can be an effective management and conservation tool but also carries the danger of eroding natural population structure, introducing non-native strains and reducing genetic diversity. Sea trout, the anadromous form of the brown trout (Salmo trutta), is a highly targeted species that is often managed by stocking. Northern Germany is characterized by short distances between the Baltic and North Sea river watersheds, historic use of fishes from both watersheds for stocking, and the creation of a potential migration corridor between the Baltic and North Sea with the opening of the Kiel Canal 120 years ago. In this study we test whether any population genetic structure persisted within and between the Baltic and North Sea after 125 year of stocking, and if so whether there is evidence of admixture between the Baltic and North Sea. We further reasoned that if such admixture were due to the opening of the Kiel Canal, it would be expected to decrease with increasing distance from the canal. If it were due to recent divergence and incomplete linage sorting between the Baltic and North Sea, it would be expected to be homogenous among Baltic river systems and among North Sea river systems. A pattern of admixture driven by stocking would in contrast be expected to present heterogeneous, river-specific patterns that reflect the idiosyncrasies of 125 years of stocking and do not correlate with distance from the Kiel Canal. Link to Conservation Genetics publication here