Comparative analysis of gut microbiome of mangrove brachyuran crabs revealed patterns of phylosymbiosis and codiversification.

ABSTRACT

The acquisition of microbial symbionts enables animals to rapidly adapt to and exploit novel ecological niches, thus significantly enhancing the evolutionary fitness and success of their hosts. However, the dynamics of host-microbe interactions and their evolutionary implications remain largely underexplored in marine invertebrates. Crabs of the family Sesarmidae (Crustacea Brachyura) are dominant inhabitants of mangrove forests and are considered keystone species there. Their rapid diversification, particularly after adopting a plant-feeding lifestyle, is believed to have been facilitated by symbiotic gut microbes, enabling successful colonization of intertidal and terrestrial environments. To investigate the patterns and mechanisms shaping the microbial communities and the role of microbes in the evolution of Sesarmidae, we characterized and compared the gut microbiome compositions across 43 crab species from Sesarmidae and other mangrove-associated families using 16S metabarcoding. We found that the gut microbiome assemblages in crabs are primarily determined by host identity, with a secondary influence from environmental factors such as microhabitat and sampling location, and to a lesser extent influenced by biological factors such as sex and gut region. While patterns of phylosymbiosis (i.e. when microbial community relationships recapitulate the phylogeny of their hosts) were consistently observed in all beta-diversity metrics analysed, the strength of phylosymbiosis varied across crab families. This suggests that the bacterial assemblages in each family were differentially shaped by different degrees of host filtering and/or other evolutionary processes. Notably, Sesarmidae displayed signals of cophylogeny with its core gut bacterial genera, which likely play crucial functional roles in their hosts by providing lignocellulolytic enzymes, essential amino acids, and fatty acids supplementation. Our results support the hypothesis of microbial contribution to herbivory and terrestrialization in mangrove crabs, highlighting the tight association and codiversification of the crab holobiont.