Assessing the Levels of Functional Adaptation: Finite Element Analysis Reveals Species, Hybrid, and Sexual Variation in the Biomechanics of African Cichlid Mandibles

Abstract

To understand how adaptive divergence emerges it is essential to examine the function of phenotypic traits along a continuum. For vertebrates, the mandible provides a key link with foraging and other important activities which has made it highly relevant for investigations of biomechanical change. Variation in mandible shape is known to correspond with ecology but its function is often only investigated between distinct species. However, for such divergence to occur and be maintained selection likely draws from many sources of biomechanical variation. African cichlids represent an exemplar model for understanding how such processes unfold with mandible variation existing between species, sexes, and is likely generated in nature by the potential for hybridization. We explored such mandible variation through a finite element modelling approach and predicted that hybrids and females would have reduced functional capabilities, the former in line with disruptive selection and the latter due to potential trade-offs incurred by maternal mouthbrooding in Malawian haplochromines. We revealed evidence of structural adaptations between Tropheops ‘Red Cheek’ and Labeotrophues fuelleborni that impacted the dispersion of mechanical stress in ways that matched the foraging of these species. Also, hybrids showed higher stresses relative to both species across the mandible. Sexual dimorphism in stress handling was evident despite minor differences in shape with males showing enhanced load resistance. However, in hybrids it appeared that males were disadvantaged relative to females, and displayed asymmetry in load handling. Together, these results show evidence of species and sex based biomechanical variation, that could be targeted by divergent selection.

Functional trait plasticity diverges between sexes in African cichlids: A contribution toward ecological sexual dimorphism?

“…weaker grouping based on foraging treatments) could be due to their highly specialised phenotype. Specifically, their phenotype enables efficient handling of mechanical stress (McWhinnie et al., 2022 ) and may in turn reduce the opportunity for bone remodelling (i.e. plasticity).…”

“…Specifically, their phenotype enables efficient handling of mechanical stress (McWhinnie et al, 2022) and may in turn reduce the opportunity for bone remodelling (i.e. plasticity).…”

“…Phenotypic plasticity is posited to play a key role in the rapid and explosive radiation of African cichlids (Gilbert, 2021;Navon et al, 2020;Parsons et al, 2016;van Snick Gray & Stauffer, 2004;Wimberger, 1992). Given previous indications of phenotypic plasticity in African cichlids (Bouton et al, 2002;Parsons et al, 2014Parsons et al, , 2016van Snick Gray & Stauffer, 2004), and evidence of sexual dimorphism consistent with ESD in mandible and craniofacial shape (McWhinnie et al, 2022;McWhinnie & Parsons, 2019), we hypothesised that plastic responses would differ between sexes of Malawi cichlids. We predicted that females of both species would display reduced plasticity relative to males as they face constraints in trophic morphology due to mouth-brooding (Tkint et al, 2012).…”