Evolution of bower building in Lake Malawi cichlid fish: phylogeny, morphology, and behavior

Abstract

Despite considerable research, we still know little about the proximate and ultimate causes behind behavioral evolution. This is partly because understanding the forces acting on behavioral phenotypes requires the study of species-rich clades with extensive variation in behavioral traits, of which we have few current examples. In this paper, we introduce the bower-building cichlids of the Lake Malawi adaptive radiation, a lineage with over 100 species, each possessing a distinct male extended phenotype used to signal reproductive fitness. Extended phenotypes are useful units of analysis for the study of behavior since they are static structures that can be precisely measured within populations. To this end we recognize two core types of bowers -mounds ("castles") and depressions ("pits"). We employ an established framework for the study of adaptive radiations to ask how traits related to other stages of radiations, macrohabitat and feeding morphology, are associated with the evolution of pit and castle phenotypes. We demonstrate that pits and castles are evolutionarily labile traits and have been derived numerous times in multiple Malawi genera. Using public ecological and phenotypic data sets we find significant and correlated differences in macrohabitat (depth), sensory ability (opsin expression), and feeding style (jaw morphology and biomechanics) between pit-digging and castle-building species. Phylogeny-corrected comparisons also show significant differences in several measures of jaw morphology while indicating non-significant differences in depth. Finally, using laboratory observations we assay courtship behaviors in a pit-digging (Copadichromis virginalis) and a castle-building species (Mchenga conophoros). Together, these results show that traits at multiple biological levels act to regulate the evolution of a courtship behavior within natural populations.

The Repeated Evolution of Behavior

“…In York et al (2015) we provide evidence that amongst the cichlid fish of Lake Malawi, Africa adaptions arising from stages (i) (macrohabitat) and (ii) (trophic style) have influenced the evolution of a courtship signal: the construction of sand mating nests or "bowers." Males of more than 100 species within the sand-dwelling lineage of Malawi cichlids seasonally build bowers in large aggregations ("leks") solely in order to attract and mate with females, a purpose almost identical to that of the eponymous bowerbirds of Oceania (Diamond, 1986;McKaye et al, 2001;Magalhaes et al, 2013).…”

“…first major feature of the landscape is that there are several of instances or repeated evolution with more than 10 conversions including the evolution of bower building in cichlid fish (likely >10 conversions; York et al, 2015) and eusociality across inverterbrates and vertebrate taxa (17 conversions; Duffy et al, 2000). A density distribution of repeated behavioral evolution instances across evolutionary time ( Figure 1B) shows a skew toward more recent evolutionary events with the majority of <100 MYA (39/49; 79.59%).…”

“…Males of more than 100 species within the sand-dwelling lineage of Malawi cichlids seasonally build bowers in large aggregations ("leks") solely in order to attract and mate with females, a purpose almost identical to that of the eponymous bowerbirds of Oceania (Diamond, 1986;McKaye et al, 2001;Magalhaes et al, 2013). Bowers are extended phenotypes that can exist in two basis form: "pits"-depressions dug out of the sand substrate-and "castles"-aggregations of sand collected from around the bower area and deposited to create a mound (Figure 2A; Dawkins, 1992;York et al, 2015). Phylogenetic analysis shows that pit and castle type bowers are evolutionarily labile.…”

Machine vision methods for analyzing social interactions

“…2B) (Branson et al, 2009;Jhuang et al, 2010) and the transition probabilities between behaviors (also called 'kinematic diagrams' or 'ethograms'; Fig. 2C) (Adamo and Hoy, 1995;Dankert et al, 2009;Seeds et al, 2014;York et al, 2015). Both time budgets and transition probabilities can be compared across species (Petru et al, 2009), strains (de Chaumont et al, 2012Kabra et al, 2013) or experimental conditions (Branson et al, 2009;Saka et al, 2004).…”

Applying gene regulatory network logic to the evolution of social behavior

“…In particular, we believe that researchers should strategically focus their efforts to study the microevolution of behavior in closely related species or different populations of the same species. There are a number of evolutionary systems where a strong foundation has already been laid, including territoriality and flocking in songbirds (71), schooling behavior in threespine stickleback fish (79), courtship and parental behaviors in African cichlid fish (80,81), aggression and schooling in blind cavefish (82,83), mating system and mating tactics in voles (84,85), and parental behavior in Peromyscus mice (86). These systems provide insight into not only the specifics of how social behavior evolves but also, the extent to which we should expect conservation of network function across much more distantly related species.…”