Open Access

Termites, the oldest eusocial insect group, display important divergent features compared to the eusocial Hymenoptera, including diploidy and an XY sex differentiation system. Termite males have frequently been shown to generate multivalent chromosome chains and rings during meiosis. This intriguing phenomenon could act on multiple evolutionary scales. Firstly, chain formation creates a higher probability of large-scale chromosomal translocations, which could play an important role in chromosome evolution across deep evolutionary time. Secondly, chains occurring in meiosis I should suppress recombination, leading to accumulation of genetic divergence in corresponding chromosomal regions, with potential consequences for speciation dynamics. Suppressed recombination may also represent a mechanism to maintain genetic heterozygosity, thereby theoretically mitigating against the negative effects of inbreeding. A high tolerance for inbreeding could have played a prominent role during the evolution of termite eusociality through its potential impact on inclusive fitness. Using newly sequenced near-chromosome-level reference genomes of native European Reticulitermes species, we will compare chromosomal translocations against other termite species as well as solitary relatives from Blattodea. Additionally, combining a large-scale population genomic data set with high resolution karyotypying across the southern European range, we aim to test the hypotheses that the occurrence and extent of chromosomal rings or chains i) are positively correlated with inbreeding, and ii) contribute to species divergence via the accumulation and fixation of genetic differences. In summary, this project seeks to identify the diverse roles that chain and ring chromosomes have played and continue to play in termite evolution.

Termites challenge long-standing assumptions about insect social evolution. One important difference compared to the social ants, bees and wasps lies in their chromosomes: termites are diploid, with X/Y sex differentiation observed in most species and males playing active roles across all castes and life stages. Adding to their uniqueness, termites exhibit multivalent chromosome chains during male meiosis—an intriguing and seldom seen feature of eukaryote evolution. These chains, in addition to other chromosomal formations, such as bivalent rings and rods, may serve to suppress recombination, thereby mitigating against the potentially harmful effects of inbreeding. Multivalent chromosome chains may also play a significant role in speciation processes by increasing the likelihood of chromosomal translocations and promoting genomic islands of divergence. In European Reticulitermes, variability in chain length and stability both between and within species provides a compelling model system for studying the evolutionary importance of multivalent chromosome chains at intra- and interspecific levels and at different evolutionary time scales. To investigate these dynamics, we collected over 200 colonies of Reticulitermes species across the Mediterranean, generating de novo reference genomes, comprehensive population genomic as well as karyotypic data from three recently diverged species. Our findings shed light on the intricate relationship between chromosomal architecture and evolutionary mechanisms in termites, offering new insight into how genome structure shapes species evolution