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Abstract

Across animals and plants, numerous metabolic and defensive adaptations
are a direct consequence of symbiotic associations with beneficial microbes.
Explaining how these partnerships are maintained through evolutionary
time remains one of the central challenges within the field of symbiosis
research. While genome erosion and co-cladogenesis with the host are
well-established features of symbionts exhibiting intracellular localization
and transmission, the ecological and evolutionary consequences of an
extracellular lifestyle have received little attention, despite a demonstrated
prevalence and functional importance across many host taxa. Using
insect–bacteria symbioses as a model, we highlight the diverse routes of
extracellular symbiont transfer. Extracellular transmission routes are unified
by the common ability of the bacterial partners to survive outside their hosts,
thereby imposing different genomic, metabolic and morphological constraints
than would be expected from a strictly intracellular lifestyle. We
emphasize that the evolutionary implications of symbiont transmission
routes (intracellular versus extracellular) do not necessarily correspond to
those of the transmission mode (vertical versus horizontal), a distinction
of vital significance when addressing the genomic and physiological
consequences for both host and symbiont.