Towards understanding the genetic basis of mouth asymmetry in the scale-eating cichlid Perissodus microlepis

How polymorphisms consisting in left–right asymmetries are produced and maintained in natural populations is a tantalizing question, which remains largely unanswered. The scale-eating cichlid fish Perissodus microlepis is a remarkable example of extreme ecological specialization achieved by morphological and behavioural laterality. Its asymmetric mouth is accompanied by a pronounced lateralized foraging behaviour, where a left-bending morph preferentially feeds on the scales of the right side of its prey, while the opposite is true for the right morph. This striking asymmetry made this fish a textbook example of the astounding degree of ecological specialization and negative frequency-dependent selection. Yet, the genetic basis underlying this spectacular laterality remains unknown. We addressed this question through analyses of wild-caught fish using high-throughput DNA sequencing data. A novel array of SNP markers was developed by ddRAD sequencing (ddRADseq) and the use of pooled DNA samples (PoolSeq). We obtained more than 155 000 SNPs using ddRADseq and 3 900 000 SNPs with PoolSeq. Among these, we identified one (ddRAD) SNP, and 38 or 378 (PoolSeq) windows that are differentiated between the left and right morphs accounting for spurious associations due to geographic structuring. This allowed us to uncover candidate genomic regions that potentially contain genes for this trait. Then, this interesting trait has a genetic basis that is likely to be influenced by multiple loci. This result contributes to a greater understanding of the genetic bases of left–right asymmetry and, ultimately, the evolutionary processes governing the maintenance of this striking case of laterality.

自然种群中左右不对称性多态性的产生与维持机制，是一个长期悬而未决且极具研究价值的核心科学问题。食鳞慈鲷小鳞奇丽鱼（Perissodus microlepis）是通过形态与行为偏侧化实现极端生态特化的典型范例：其不对称的口部伴随显著的偏侧化觅食行为，左弯形态型优先取食猎物右侧的鳞片，右弯形态型则反之。这种鲜明的不对称性使其成为生态特化与负频率依赖选择（negative frequency-dependent selection）惊人程度的经典研究案例。然而，该物种显著偏侧化现象的遗传基础仍未被揭示。本研究通过对野生捕获个体的高通量DNA测序数据分析，解答了这一科学问题：我们利用双酶切限制性位点相关DNA测序（ddRADseq）与混合DNA样本测序（PoolSeq）技术，开发了一套全新的单核苷酸多态性（Single Nucleotide Polymorphism, SNP）标记阵列。其中，通过ddRADseq技术我们获得了超过155,000个SNP位点，PoolSeq技术则得到了390万个SNP位点。在此基础上，我们校正了由地理结构引发的假关联后，筛选出左、右形态型间存在分化的遗传区域：ddRAD技术鉴定出1个差异SNP位点，PoolSeq技术则鉴定出38个或378个差异基因组窗口。这一结果使我们得以挖掘出可能携带该性状相关基因的候选基因组区域，表明该有趣性状的遗传基础极有可能受多个基因座共同调控。本研究结果有助于我们更深入地理解左右不对称性的遗传基础，并最终阐明维持这种显著偏侧化现象的进化机制。