A new study reveals that exposing dwarf spiders to a brief period of warm temperatures can disrupt a phenomenon where internal bacteria normally force genetic males to develop as females. Surprisingly, this reproductive disruption skips the directly heated spiders and hits their children and grandchildren instead, leading to a sudden comeback of male offspring. The temporary heat scrambles the spiders' internal microscopic ecosystem, allowing a rival bacterium to surge ahead and block the feminizing bacteria from taking over.
A single brief spell of warm weather can ripple across generations, altering the internal bacterial ecosystems of spiders and disrupting their reproduction, according to a study from Israeli and American researchers.
The research, published in Molecular Ecology, was led by Prof. Yuval Gottlieb-Dror and the PhD student Virginija Mackevicius-Dubickaja from the Koret School of Veterinary Medicine at the Hebrew University of Jerusalem, alongside collaborators, Prof. Jen White from the University of Kentucky and Prof. Matt Duremos from the University of Illinois. The team investigated the dwarf spider (Mermessus fradeorum), an arthropod that naturally carries up to five different types of maternally transmitted bacteria inside its body.
One of these bacteria, a strain of Wolbachia, forces genetic male spiders to develop as females—a phenomenon known as feminization. This strategy allows the bacteria to spread rapidly, since they are passed down directly from mothers to their offspring. However, in nature, these feminizing bacteria only exist at intermediate frequencies, prompting scientists to investigate what constrains their spread.
To test the impact of temperature, the researchers exposed young spiders to elevated conditions mimicking warm summer daytime surface temperatures (27°C to 28°C) for just one generation. While the heat-exposed spiders themselves grew up into females as expected, a delayed effect occurred when they laid eggs back in a standard, cool environment (20°C).
Their children and grandchildren, who never directly experienced the heat, exhibited a disrupted feminization process, resulting in a sudden return of male offspring.
The scientists discovered that the temporary heat exposure triggered a transgenerational shift in the spiders' internal microbial dynamics. While the feminizing Wolbachia initially increased in titre under the heat, its ability to transmit successfully into the next generation declined. Concurrently, another resident bacterium called Tisiphia was completely lost from the lineage.
These shifts coincided with a surge in a rival bacterium, Rickettsiella, in the subsequent generation. The data demonstrated that a high relative abundance of Rickettsiella is negatively associated with feminization, suggesting it acts as an antagonist that suppresses Wolbachia.
"Our findings demonstrate how an organism's environmental history shapes the evolutionary stability of its microbial communities and their induced phenotypes," said the researchers. "A brief period of elevated temperatures disrupts the delicate competitive balance between these symbionts. We observed that Rickettsiella appears to inhibit the feminization process, showing that reproductive manipulation requires not just the presence of Wolbachia, but its relative dominance within the microbial community."
The study also found that spiders carrying multiple strains of Wolbachia (strains 1, 2, and 3) were much more resilient, maintaining stable symbiont relative abundances and recovering their female-heavy sex ratios faster than those with fewer strains. This indicates that co-infection enhances the stability of symbiont dynamics under thermal stress.
The results offer a real-time observation of how environmental conditions destabilize natural microbial communities within a live host. In natural populations experiencing daily and seasonal thermal fluctuations, environmentally driven shifts in symbiont communities likely influence transmission efficiency and host population structure. By occasionally reducing feminization rates, thermal stress may act as an important mechanism for maintaining males within the population and avoiding a demographic collapse.
