Sympatric or micro-allopatric speciation in a glacial lake? Genomic islands support neither

Ning Sun; Liandong Yang; Fei Tian; Honghui Zeng; Ziwen He; Kai Zhao; Cheng Wang; Minghui Meng; Chenguang Feng; Chengchi Fang; Wenqi Lv; Jing Bo; Yongtao Tang; Xiaoni Gan; Zuogang Peng; Yiyu Chen; Shunping He

doi:10.1093/nsr/nwac291

Sympatric or micro-allopatric speciation in a glacial lake? Genomic islands support neither

Natl Sci Rev. 2022 Dec 27;9(12):nwac291. doi: 10.1093/nsr/nwac291. eCollection 2022 Dec.

Authors

Ning Sun^{1

2}, Liandong Yang¹, Fei Tian³, Honghui Zeng¹, Ziwen He⁴, Kai Zhao³, Cheng Wang^{1

2}, Minghui Meng¹, Chenguang Feng^{1

5}, Chengchi Fang¹, Wenqi Lv^{1

2}, Jing Bo^{6

2}, Yongtao Tang³, Xiaoni Gan¹, Zuogang Peng⁷, Yiyu Chen⁸, Shunping He^{1

6

9}

Affiliations

¹ State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China.
² University of Chinese Academy of Sciences, Beijing 100049, China.
³ Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810008, China.
⁴ State Key Laboratory of Biocontrol, Guangdong Key Lab of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China.
⁵ School of Ecology and Environment, Northwestern Polytechnical University, Xi'an 710129, China.
⁶ Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China.
⁷ Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Southwest University School of Life Sciences, Chongqing 400700, China.
⁸ National Natural Science Foundation of China, Beijing 100085, China.
⁹ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China.

Abstract

Apparent cases of sympatric speciation may actually be due to micro-allopatric or micro-parapatric speciation. One way to distinguish between these models is to examine the existence and nature of genomic islands of divergence, wherein divergent DNA segments are interspersed with low-divergence segments. Such islands should be rare or absent under micro-allopatric speciation but common in cases of speciation with gene flow. Sympatric divergence of endemic fishes is known from isolated saline, crater, postglacial, and ancient lakes. Two morphologically distinct cyprinid fishes, Gymnocypris eckloni scoliostomus (GS) and G. eckloni eckloni (GE), in a small glacial lake on the Qinghai-Tibet Plateau, Lake Sunmcuo, match the biogeographic criteria of sympatric speciation. In this study, we examined genome-wide variation in 46 individuals from these two groups. The divergence time between the GS and GE lineages was estimated to be 20-60 Kya. We identified 54 large genomic islands (≥100 kb) of speciation, which accounted for 89.4% of the total length of all genomic islands. These islands harboured divergent genes related to olfactory receptors and olfaction signals that may play important roles in food selection and assortative mating in fishes. Although the genomic islands clearly indicated speciation with gene flow and rejected micro-allopatric speciation, they were too large to support the hypothesis of sympatric speciation. Theoretical and recent empirical studies suggested that continual gene flow in sympatry should give rise to many small genomic islands (as small as a few kilobases in size). Thus, the observed pattern is consistent with the extensive evidence on parapatric speciation, in which adjacent habitats facilitate divergent selection but also permit gene flow during speciation. We suggest that many, if not most, of the reported cases of sympatric speciation are likely to be micro-parapatric speciation.

Keywords: gene flow; genomic islands; micro-parapatric speciation; olfaction; selection; sympatric speciation.