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Origin of a complex key innovation in an obligate insect-plant mutualism.

ABSTRACT: Evolutionary key innovations give organisms access to new ecological resources and cause rapid, sometimes spectacular adaptive radiation. The well known obligate pollination mutualism between yuccas and yucca moths is a major model system for studies of coevolution, and it relies on the key innovation in the moths of complex tentacles used for pollen collecting and active pollination. These structures lack apparent homology in other insects, making them a rare example of a novel limb. We performed anatomical and behavioral studies to determine their origin and found evidence of a remarkably simple mechanism. Morphological analyses of the tentacles and adjacent mouthparts in pollinators and closely related taxa showed that the tentacle appears abruptly in female pollinating yucca moths. Several morphological synapomorphies between the galeae, which constitute the characteristic lepidopteran proboscis, and the tentacle suggest that the tentacle evolved quickly through expression of the genetic template for the galea at an apical growth bud on the first segment of the maxillary palp. Behavioral data indicate that tentacle and proboscis movements are controlled by a shared hydraulic extension mechanism, thus no new mechanism was needed for tentacle function. Known developmental paths from other insects can explain the origin of this sex-specific key innovation in a few steps.

SUBMITTER: Pellmyr O

PROVIDER: S-EPMC122798 | biostudies-literature | 2002 Apr

REPOSITORIES: biostudies-literature

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Origin of a complex key innovation in an obligate insect-plant mutualism.

Pellmyr Olle O Krenn Harald W HW

Proceedings of the National Academy of Sciences of the United States of America 20020401 8

Evolutionary key innovations give organisms access to new ecological resources and cause rapid, sometimes spectacular adaptive radiation. The well known obligate pollination mutualism between yuccas and yucca moths is a major model system for studies of coevolution, and it relies on the key innovation in the moths of complex tentacles used for pollen collecting and active pollination. These structures lack apparent homology in other insects, making them a rare example of a novel limb. We perform ...[more]

PMID: 11960006

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Project description:Mutualism between long corolla tubed plants and their potential pollinators, long-tongued flies, is a classic example of coevolution, but to date, has only been reported from the regions of southern Africa. Many plant species from the Himalayas also show botanical characteristics that could be consistent with pollination by long-tongued flies. Here, we seek the evidence of the "long-tongued-long tubed fly/flower" mutualism out of Africa, in a different continent and climatic region, the Himalayas.Floral traits of Himalayan region endemic alpine genus, Roscoea, indicate possible mutualism with long-tongued flies for pollination success; however, effective pollinators of this genus are yet unknown. This study investigates whether long-tongued flies and Roscoea purpurea in Nepal Himalayas show exclusive mutualism for their survival/reproduction.We made extensive observations of floral visitors of R. purpurea and food source of Philoliche longirostris across their wide ranges of populations in Nepal Himalayas for three consecutive years (2012-2014). To confirm the obligate reliance of R. purpurea upon P. longirostris for pollination success, manipulated pollination experiments were conducted at two populations for 2 years. Similarly foraging behavior, visitation frequency, and pollination efficiency of P. longirostris were assessed at two populations for 2 years, and its contribution for the reproductive success of R. purpurea was evaluated. Our results indicate that R. purpurea is self-compatible but lacks autonomous selfing and obligatorily relies on P. longirostris for reproductive success. Across all populations, P. longirostris was observed as an exclusive and highly efficient pollinator of R. purpurea, while P. longirostris exclusively depends up on R. purpurea for food source.Out of Africa, this study provides the first evidence of long-tongued fly pollination system and indicates the possibility of additional instances of such a rare phenomenon in the Himalayas. Finding of specialized pollinator of Roscoea only at its evolutionary center indicates that Roscoea species are originally pollinated by long-tongued flies. Spatial mismatch with specialized pollinators may have induced the evolution of autonomous selfing in North Indochinese clades of Roscoea. This finding thus substantiates how geographic disjunction causes the shifting of pollination mechanism in closely related plant species.

Dataset Information

Origin of a complex key innovation in an obligate insect-plant mutualism.

Publications

Origin of a complex key innovation in an obligate insect-plant mutualism.

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