How are species boundaries maintained in the face of environmental disturbance? This is not only a fundamental question in evolutionary biology but also an increasingly important one as human activities and climate change alter habitats and bring previously separated species into contact.
As mechanisms preventing gene exchange between populations, known as reproductive isolation, accumulate, populations can eventually diverge into separate species. When reproductive isolation is incomplete, however, environmental changes can bring closely related species into contact and lead to hybridization. For species boundaries to persist despite extensive hybridization, much of the genomic regions introduced from another species must be eliminated. Yet how rapidly this process occurs in nature, and which reproductive isolation mechanisms contribute to the removal of foreign genomic regions, have remained poorly understood.
The tsunami triggered by the Great East Japan Earthquake in 2011 dramatically altered habitats along the Pacific coast of northeastern Japan. Otsuchi Town in Iwate Prefecture was struck by a tsunami exceeding 10 meters in height. The tsunami and subsequent backwash are thought to have brought the marine Japan Sea stickleback, Gasterosteus nipponicus, from the sea and a freshwater population of the threespine stickleback, Gasterosteus aculeatus, from upstream into newly formed freshwater habitats in the town center. This brought the two closely related fish species into contact and resulted in interspecific hybridization.
A research team comprising scientists from the National Institute of Genetics (NIG), Hokkaido University, Gifu Kyoritsu University, Kyoto University, Ishinomaki Senshu University, Nagoya University, Keio University, The University of Tokyo, and Tokyo University of Marine Science and Technology tracked this hybrid population for nine years. In 2012, 38% of the individuals sampled were hybrids. Over the following years, however, genomic regions derived from G. nipponicus rapidly declined across the genome, and by 2020 the population had returned to an almost entirely G. aculeatus genomic composition. Because the generation time of this population is approximately one year, most of the G. nipponicus-derived genome was eliminated within about 10 generations.
Genomic regions containing major reproductive isolation loci associated with freshwater adaptation, migration to the sea, mate choice, and hybrid male sterility showed particularly rapid declines in G. nipponicus ancestry. However, these major loci alone could not explain the genome-wide removal observed over 10 generations. Individual-based simulations suggested that numerous weak genetic incompatibilities distributed throughout the genome may also have contributed to the rapid elimination of G. nipponicus ancestry.
"There were two major surprises in this study," said Takuya Hosoki and Jun Kitano. "First, we did not expect genomic regions associated with major reproductive barriers to be purged so rapidly. Second, we were surprised that most of the foreign genome continued to disappear over subsequent generations. An important next question is whether this combination of a few strong reproductive barriers and many weak genetic incompatibilities represents a general mechanism by which species boundaries are maintained after hybridization."
This study is one of the few to track genomic changes in a natural population from immediately after interspecific hybridization through approximately 10 generations. By directly observing the progressive removal of foreign genomic regions, the study reveals how multiple reproductive barriers can work together to maintain species boundaries following extensive hybridization.
About National Institute of Genetics (NIG)
National Institute of Genetics (NIG) was established to carry out broad and comprehensive research in genetics. NIG contributes to the development of academic research as one of the inter-university research institutes constituting the Research Organization of Information and Systems (ROIS).
About the Research Organization of Information and Systems (ROIS)
ROIS is a parent organization of four national institutes (National Institute of Polar Research, National Institute of Informatics, the Institute of Statistical Mathematics and National Institute of Genetics) and the Joint Support-Center for Data Science Research. It is ROIS's mission to promote integrated, cutting-edge research that goes beyond the barriers of these institutions, in addition to facilitating their research activities, as members of inter-university research institutes.
