Research

Recent evolutionary radiations such as Darwin’s finches, East African cichlids or Heliconius butterflies have served as model systems to understand how novel variation and new species arise. These systems, clearly in the early stages of divergence, have stimulated research into the behavioral, ecological, and genetic bases of reproductive isolation that have arguably transformed our understanding of the origins of biodiversity. However, no analogous classic radiation comes to mind in the largest ecosystem on earth, the ocean. The overarching goal of our research is to develop the hamlets (Hypoplectrus spp, Serranidae, photographs below), simultaneously hermaphroditic reef fishes from the wider Caribbean, into a model system for the study of marine speciation.

The hamlets are diverse, with a variety of color patterns and geographic distributions that provide the opportunity to repeat comparisons both taxonomically and geographically. They encapsulate the entire spectrum of divergence, from genomic similarity to well-diverged species. Mate choice and spawning can be directly observed in the field throughout the year, providing a handle on reproductive isolation which surpasses nearly any other marine group for the sheer number and quality of behavioral observations that can be made in natural populations. Color pattern has been identified as an important ecological trait that is also used for mate choice, and specific hypotheses regarding the role played by natural and sexual selection in speciation have been developed. Finally, a number of genomic resources are available for the group.

Interests

  • Marine speciation
  • Local adaptation
  • Sexual selection
  • Recombination
  • Dispersal
  • Genomics
  • Behavior
  • Theory

Ongoing projects

  • Genomic architecture of speciation

    With the advent of second and third generation DNA sequencing technologies, we have entered a new phase of biological exploration in which natural populations can be assayed for the genomic signatures of speciation, providing the opportunity to identify the patterns and processes leading to genomic divergence. We are assembling a chromosome-level reference genome for Hypoplectrus and resequencing full genomes to address the following questions: (i) What is the genomic architecture of speciation, and how does it evolve along the speciation continuum? (ii) What are the genomic elements underlying species differences, and do their evolutionary history differ from the rest of the genome? (iii) How repeatable are patterns of genomic divergence? (iv) Does speciation proceed in the presence of gene flow? Led by Kosmas Hench, funded by the DFG, Smithsonian Institute for Biodiversity Genomics and Global Genome Initiative.

  • Behavioral syndromes and reproductive isolation

    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 Sophie Picq, funded by IMPRS through GEOMAR and a short-term fellowship from the Smithsonian Tropical Research Institute.

  • Evolution of egg trading

    Hermaphroditism is estimated to occur in about 65,000 animal species distributed over 70% of animal phyla, which represents a third of animal species excluding insects. A significant proportion of hermaphrodites are simultaneous hermaphrodites, which sets the stage for self-fertilization and egg trading, whereby individuals reciprocally fertilize each other’s eggs. Egg trading is of particular interest because it has been suggested to represent a rare case of cooperation among unrelated individuals and to stabilize simultaneous hermaphroditism. Nevertheless, egg trading remains a rarity among simultaneous hermaphrodites, having been reported in a restricted number of polychaete, sea slug and fish species only. While previous studies have addressed the stability of egg trading once established, how it may initially invade a population of non-trading simultaneous hermaphrodites remains an open question. Here, we tackle this problem with an analytical model that considers explicitly encounter rates and costs of egg production in a population that may include non-traders (who provide eggs at every mating opportunity), traders (who provide eggs only if their partners also do so) and cheaters (who never provide eggs and only mate in the male role). Led by Jorge Peña in collaboration with Dr. Georg Nöldeke, funded by The Future Ocean.

  • Maya hamlet conservation genomics

    The recently described Maya hamlet (Hypoplectrus maya), endemic to the coastal lagoon of the Belize Barrier Reef, appears to have severely declined during the last  decades. In this project we leverage the power of full-genome data to reconstruct the evolutionary history of this atypical species, estimate its effective population size and establish whether it needs to be protected. Led by Ben Moran, funded by the National Geographic Society, Northeastern University and DFG.

  • Color patterns in coral reef fishes

    The colors patterns displayed by coral reef fishes are among the most visually stunning traits in animals, but they are notoriously difficult to analyze and quantify objectively. Using the hamlets as a model system, we are developing a pipeline to quantify both color and patterns in coral reef fishes. This project involves fieldwork, high-resolution photography, spectrophotometry, image analysis as well as a citizen science component whereby scuba divers are invited to send us their hamlet photographs. Led by Derya Akkaynak and Kosmas Hench, funded by The Future Ocean and GEOMAR.

  • Matching theory, mutual mate choice and speciation

    The award of the 2012 Nobel Prize in Economic Sciences to the two main founders of matching theory, Alvin E. Roth and Lloyd S. Shapley, establishes the fundamental importance and specificity of this theoretical framework. In evolutionary biology, matching theory provides a very distinctive opportunity to address sexual selection and speciation in a context of mutual mate choice. We are using matching theory to explore the role played by mutual mate choice in speciation. Led by Sophie Picq, funded by IMPRS through GEOMAR.

  • Genomic architecture of local adaptation

    Whether populations are adapted to local conditions, and if so through what mechanisms, are fundamental questions in evolutionary ecology. This is particularly true in the marine environment, where absolute barriers to the movement of organisms are few and planktonic larval stages provide potential for extensive dispersal. Are marine populations able to adapt to local environmental conditions in such a potentially high gene-flow context? This is not only a basic question but also an applied one, as the occurrence of locally adapted marine populations has far-reaching implications for management, conservation, and the ability to cope with global change. We are resequencing hamlet genomes from a variety of locations across the wider Caribbean to address this question. Led by O. Puebla, funded by the lab.

  • Population genetic structure after 125 years of stocking in sea trout

    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. Led by Christoph Petereit.

  • Marine Protected Areas and artisanal fisheries

    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 as key conservation and management tools to sustain marine resources and artisanal fisheries through adult spillover and larval dispersal beyond their boundaries. 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. Briefly, the idea is to assess the effect of MPAs on artisanal fisheries, going from population genetics and physical oceanography to the socio-economics of artisanal fisheries. Led by Katharina Fietz and Siren Rühs in collaboration with Stéphanie Manel and Arne Biastoch.

Finalized projects

  • Recombination in the eggs and sperm

    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.

  • Hamlet community dynamics

    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 JFB publication here.