Behavioral evolution contributes to hindbrain diversification among Lake Malawi cichlid fish

Abstract

The evolutionary diversification of animal behavior is often associated with changes in the structure and function of nervous systems. Such evolutionary changes arise either through alterations of individual neural components (“mosaically”) or through scaling of the whole brain (“concertedly”). Here we show that the evolution of a courtship behavior in Malawi cichlid fish is associated with rapid, extensive, and specific diversification of orosensory, gustatory centers in the hindbrain. We find that hindbrain volume varies significantly between species that build pit (depression) compared to castle (mound) type bowers and that this trait is evolving rapidly among castle-building species. Molecular analyses of neural activity via immediate early gene expression indicate a functional role for hindbrain structures during bower building. Finally, comparisons of bower building species in neighboring Lake Tanganyika suggest parallel patterns of neural diversification to those in Lake Malawi. Our results suggest that mosaic brain evolution via alterations to individual brain structures is more extensive and predictable than previously appreciated.

A connectomics-based taxonomy of mammals

“…Accordingly, inter-species differences in functional and behavioural repertoire are likely supported by changes in local connectivity patterns. Along the same lines, our results are also consistent with the notion that neural circuit evolution involves random local circuit modifications that may have provided species with behavioural adaptations, allowing them to face specific challenges ( Barker, 2021 ), such as extreme environmental pressures Park et al, 2008 ; Smith et al, 2011 ; Eigenbrod et al, 2019 , or to support specific behaviours, such as courtship ( O’Grady and DeSalle, 2018 ; Markow and O’Grady, 2005 ; Ding et al, 2019 ; Seeholzer et al, 2018 ; Khallaf et al, 2020 ; Barkan et al, 2018 ; Ding et al, 2016 ; York et al, 2019 ), social bonding ( Insel and Shapiro, 1992 ; Winslow et al, 1993 ; Jaggard et al, 2020 ; Loomis et al, 2019 ), or foraging ( Vanwalleghem et al, 2018 ; Pantoja et al, 2020 ). How computations and cognitive functions emerge from these species-specific circuit modifications remains a key question in the field ( Buckner and Krienen, 2013 ; Suárez et al, 2021 ).…”

A connectomics-based taxonomy of mammals

“…Accordingly, inter-species differences in functional and behavioural repertoire are likely supported by changes in local connectivity pat-terns. Along the same lines, our results are also consistent with the notion that neural circuit evolution involves local circuit modifications to adapt to specific challenges [10], such as extreme environmental pressures [36,75,84], or to support specific behaviours, such as courtship [9,34,35,47,58,73,82,107], social bonding [45,46,53,103], or foraging [74,99]. How computations and cognitive functions emerge from these speciesspecific circuit modifications remains a key question in the field [22,90].…”

Evolution of regulatory networks associated with traits under selection in cichlids

“…Considering the smaller divergence time of the three haplochromines (~ 6 MYA) and the three haplochromines vs O. niloticus (~ 19 MYA) [ 47 ], this indicates gene expression divergence over different evolutionary timescales and co-expression of different clusters of genes across species. Given that the volumes and, hence, representation of region-specific cell types of selected organ, e.g., brain regions can be different, even between closely related cichlids [ 48 ], it is plausible that the observed expression differences between species are driven by changes in cell type abundances. However, given that expression data was generated from the organs of multiple similarly sized adult individuals and the identification of conserved tissue-specific patterns across all tissues and species, e.g., module 1 is eye specific (Fig.…”