Pollination niche shifts in sympatric globular cacti Eriosyce: Consequences on reproductive isolation and species formation

Pablo C Guerrero; Jaime Martínez-Harms; Mary T K Arroyo; Deren Eaton; Beatriz M Meriño; Antonio Varas-Myrik; Heidy M Villalobos-Barrantes; Gastón O Carvallo

doi:10.1016/j.pld.2025.03.001

Pollination niche shifts in sympatric globular cacti Eriosyce: Consequences on reproductive isolation and species formation

Plant Divers. 2025 Mar 11;47(3):440-453. doi: 10.1016/j.pld.2025.03.001. eCollection 2025 May.

Authors

Pablo C Guerrero^{1

2

3}, Jaime Martínez-Harms⁴, Mary T K Arroyo^{2

5

6}, Deren Eaton⁷, Beatriz M Meriño^{1

2}, Antonio Varas-Myrik⁸, Heidy M Villalobos-Barrantes^{1

9

10}, Gastón O Carvallo^{2

11}

Affiliations

¹ Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, 4030000, Concepción, Chile.
² Institute of Ecology and Biodiversity (IEB), Las Palmeras 3425, Ñuñoa, 7800003, Santiago, Chile.
³ Millennium Institute Biodiversity of Antarctic and Sub-Antarctic Ecosystems (BASE), 7800003, Santiago, Chile.
⁴ Instituto de Investigaciones Agropecuarias, INIA-La Cruz, 2280000, La Cruz, Chile.
⁵ Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, 7800003, Santiago, Chile.
⁶ Cape Horn International Center (CHIC), O'Higgins 310, 6350000, Puerto Williams, Chile.
⁷ Department of Ecology, Evolution and Environmental Biology, Columbia University, 10027, New York, USA.
⁸ Centro Intihuasi, Instituto de Investigaciones Agropecuarias, La Serena, Chile.
⁹ Centro de Investigación en Biología Celular y Molecular, Universidad de Costa Rica, 11501-2060, San José, Costa Rica.
¹⁰ Escuela de Química, Universidad de Costa Rica, 11501-2060, San José, Costa Rica.
¹¹ Instituto de Biología, Facultad de Ciencias, Pontificia Universidad Católica de Valparaíso, 2373223, Valparaíso, Chile.

Abstract

Pollination niches, which encompass the factors influencing pollen exchange among angiosperms, are fundamental to understanding reproductive success and the intricate eco-evolutionary dynamics of plants. In this study, we investigated pollination niche shift among four sympatric Eriosyce cacti with restricted distributions in the South American Mediterranean region. Utilizing a comprehensive approach-including pollination niche analysis, pollinator color perception studies, reproductive output assessments, molecular phylogenetics, gene flow analyses, and species distribution modeling-we revealed a significant pollination niche displacement in E. chilensis and its variety, E. chilensis var. albidiflora. These taxa transitioned from a hummingbird-pollinated system prevalent in the Eriosyce sect. Neoporteria, characteristic of their sister species E. litoralis, to a bee-pollination strategy akin to that of the co-occurring species E. mutabilis. This shift highlights a simultaneous convergence of E. chilensis toward E. mutabilis and divergence from E. litoralis in pollination strategies, providing adaptive advantages by reducing pollen limitation and enhancing seed production. The morphological and flowering phenological similarities between E. chilensis and E. mutabilis suggest the evolution of a shared advertising display, potentially indicative of floral mimicry, wherein both species benefit from attracting shared bee pollinators. Genomic analyses reveal distinct pollinator-driven selection pressures, with E. chilensis/E. albidiflora exhibiting traits that promote reproductive isolation from E. litoralis, supporting a scenario of rapid speciation occurring within the past half of million years in the absence of geographic barriers. These findings underscore the pivotal role of pollinator interactions in shaping angiosperm speciation and biodiversity, highlighting their dynamic influence on ecological and evolutionary processes.

Keywords: Cactaceae; Ecological divergence; Gene flow; Mediterranean biome; Pollination; Sexual selection.