Gene flow and habitat heterogeneity shape coexistence dynamics of Arctic charr morphs in connected lakes

Sympatric morphs provide valuable systems for studying incipient
divergence despite incomplete reproductive isolation. In connected
waterbodies with spatially heterogeneous habitats, one or more morphs may
form metapopulation structures, generating eco-evolutionary dynamics
unlike those in single lakes. We studied the phenotypic and genome-wide
differentiation in Arctic charr (Salvelinus alpinus) in two Icelandic
lakes (Thingvallavatn, known to harbour four distinct morphs, and a
smaller downstream lake, Ulfljotsvatn), using geometric morphometrics,
diet analysis, genome-wide SNPs acquired via double digest
Restriction-site Associated DNA sequencing (ddRADseq) and two
morph-associated mitochondrial markers. Our analyses confirm a single
origin of charr polymorphism in this system, with all morphs present in
both lakes. Relative morph abundances differ between the lakes: PL-charr
dominate in Thingvallavatn, whereas LB-charr are most abundant in
Ulfljotsvatn. Three morphs, large- (LB-), small (SB-) benthivorous and
planktivorous (PL-) charr, are genetically distinct. The system likely
forms a source-sink structure for both PL- and SB-charr, though migration
rates from Thingvallavatn vary remarkably, resulting in distinct
population dynamics. Conversely, LB-char exhibit genetic differentiation
between the lakes, suggesting the presence of a separate population in
Ulfljotsvatn. While piscivorous (PI-) charr appear genetically similar to
PL-charr, evidence suggests hybridization between PI- and LB-charr in both
lakes. Moreover, the higher hybridization in the downstream lake likely
contributes to the observed erosion of genetic separation between LB- and
PL-charr in Ulfljotsvatn. These findings suggest that the complex
interplay of habitat heterogeneity and morph-specific migrations shapes
the coexistence and eco-evolutionary dynamics of sympatric charr morphs in
the connected lakes. Our study highlights the importance of investigating
early divergence in spatially complex systems to advance eco-evolutionary
research.

尽管生殖隔离尚未完全形成，同域形态（sympatric morphs）仍是研究物种初期分化的极具价值的研究体系。在生境空间异质性显著的连通水体中，一种或多种同域形态可形成集合种群（metapopulation）结构，进而产生与单一生境湖泊截然不同的生态-进化动态。本研究以冰岛的两处连通湖泊——已知存在四种独特同域形态的辛格瓦德拉湖（Thingvallavatn）以及下游小型湖泊乌尔夫约茨湖（Ulfljotsvatn）中的北极红点鲑（Arctic charr，*Salvelinus alpinus*）为研究对象，采用几何形态测量法、饮食分析、通过双酶切限制性位点关联DNA测序（double digest Restriction-site Associated DNA sequencing, ddRADseq）获得的全基因组单核苷酸多态性（single nucleotide polymorphism, SNPs），以及两种与形态相关的线粒体标记，对其表型分化与全基因组分化水平展开研究。本研究分析证实，该研究体系内红点鲑的多态性起源单一，且所有形态均同时存在于两处湖泊中。两处湖泊的形态相对丰度存在显著差异：辛格瓦德拉湖以PL-红点鲑占主导，而乌尔夫约茨湖则以LB-红点鲑为优势类群。三类形态——底食性的大型（LB-）、小型（SB-）红点鲑以及浮游生物食性（PL-）红点鲑——在遗传层面存在显著分化。尽管从辛格瓦德拉湖向外的迁移率存在显著差异，导致种群动态各不相同，但该体系对于PL-与SB-红点鲑而言，大概率形成了源-汇种群结构。与之相反，LB-红点鲑在两处湖泊间存在遗传分化，这表明乌尔夫约茨湖内存在独立的LB-红点鲑种群。尽管食鱼性（PI-）红点鲑在遗传层面与PL-红点鲑较为相似，但已有证据表明，两处湖泊中均存在PI-与LB-红点鲑的杂交事件。此外，下游湖泊中更高的杂交频率，或许正是造成乌尔夫约茨湖内LB-与PL-红点鲑遗传分化程度降低的原因。上述研究结果表明，生境异质性与形态特异性迁移之间的复杂互作，塑造了连通湖泊中同域红点鲑形态类群的共存模式与生态-进化动态。本研究强调，对空间结构复杂的体系中的物种早期分化展开研究，对于推动生态-进化领域的研究发展具有重要意义。