Early life disruption of the microbiota affects organ development and cytokine gene expression in threespine stickleback

Abstract

The microbiota that inhabits vertebrates exerts strong effects on host physiology and can be crucial to the development of a normal phenotype. This includes development of the immune system, somatic growth and maintenance, and morphogenesis. However, the genetic background of the host can also affect these life history traits. To this end, we investigated the effects of the microbiota on growth, development, and immune gene expression on two populations of threespine stickleback (Gasterosteus aculeatus), one anadromous and one freshwater. We tested the hypotheses that microbial colonization and the genetic background of the host would affect survival, cytokine gene expression, growth, and development. We raised in vitro crosses of stickleback larvae with and without conventional microbiota. We then exposed all these treatments to Vibrio anguillarum, a potential fish pathogen, in a full factorial design. We found stickleback raised without conventional microbiota had smaller swim bladders relative to those raised with conventional microbiota. Stickleback raised with conventional microbiota exhibited small increases in cytokine gene expression. We found no differences in growth or survival regardless of treatment. These results are consistent with other investigations that show microbiota disruption, in early life, can alter host organ and tissue development and immune responses.

Fig. 1

An overview of the full factorial design (A) and the timeline (B) of the experiment. Each flask contained 40 stickleback.

Fig. 2

The morphological measurements of 14 dpf threespine stickleback.

Fig. 3

Least square means (±1 SE) of morphological measurements, eye diameter (A), swim bladder length (B), and swim bladder area (C), from anadromous (Rabbit Slough) and freshwater (Westchester Lagoon) stickleback by microbiota and V. anguillarum exposure. Least square means are from a linear mixed model with SVL as a covariate.

Fig. 4

Normalized relative expression of cytokine genes IL-β (A) and TNF-α (B) from anadromous (Rabbit Slough) and freshwater (Westchester Lagoon) stickleback by microbiota and V. anguillarum exposure. Lines inside boxes indicate medians, boxes indicate 25th and 75th percentiles, bars indicate 1.5 × interquartile range, and points are individual measurements.