BMAA in cycad-feeding Lepidoptera: defensive sequestration or bioaccumulation?

Abstract

Many herbivorous Lepidoptera accumulate plant toxins within their own tissues as a defensive strategy. Pioneering research in this area was conducted by Miriam Rothschild and Deane Bowers, who showed that the cycad-feeding butterfly Eumaeus atala sequester the toxic plant compound cycasin and thereby deter vertebrate and invertebrate predators. The current study focuses on another cycad compound, β-methylamino-L-alanine (BMAA), that is known to accumulate in the tissues of insects and other herbivores, and which has been shown to have neurotoxic effects in humans. Chemical analyses revealed that BMAA accumulates in both immature and adult tissues of E. atala, as well as adult tissues of another cycad-feeding lepidopteran, Seirarctia echo. However, the distribution of BMAA across life stages and tissues did not conform to patterns predicted for defensive sequestration, and subsequent behavioral experiments with ants showed that these invertebrate predators were not deterred by BMAA. Our results suggest that high levels of BMAA in the tissues of cycad-feeding insects likely reflect passive bioaccumulation rather than defensive sequestration. Combined with the previous work by Rothschild and Bowers, these results provide an example in which two different plant toxins accumulate within the tissues of a single herbivore species via different mechanisms and with different implications for ecology and evolution. They thereby lay the groundwork for further investigation into the processes underlying active sequestration and non-adaptive bioaccumulation.

New insights on cycad biology and evolution

“…Some cycad-feeding Aulacoscelinae beetles reflexively bleed MAM-glycosides -presumably sequestered from their foodplantswhen disturbed or threatened (Prado et al, 2011), and at least one lepidopteran has been shown to be capable of detoxifying MAM (Teas, 1967). Recently, the obligate cycad herbivore Eumaeus atalabutterfly was found to accumulate BMAA into their larval and adult tissues (Whitaker et al ., 2023), although the defensive value of sequestering BMAA remains questionable given its latent toxicity (Whitaker et al, 2022). Genomic evidence does suggest, however, that toxin tolerance is a key adaptation in the radiation ofEumaeus butterflies, a wholly cycadivorous neotropical genus of six species (Robbins et al, 2021).…”