Absence asymmetry: the evolution of monorchid beetles (Insecta: Coleoptera: Carabidae).

Department of Environmental Science, Policy and Management, Division of Insect Biology, University of California, Berkeley, California 94720, USA. kiplingw@nature.berkeley.edu

Asymmetrical monorchy, or the complete absence of one testis coupled with the presence of its bilateral counterpart, is reported for 174 species of the carabid beetle tribes Abacetini, Harpalini, and Platynini (Insecta: Coleoptera: Carabidae) based on a survey of over 820 species from throughout the family. This condition was not found in examined individuals of any other carabid beetle tribes, or of other adephagan beetle families. One monorchid taxon within Platynini exhibits symmetrical vasa deferentia at the beginning of the pupal stadium, suggesting that developmental arrest of the underdeveloped vas deferens takes place in pupation. The point at which development of the testis is interrupted is unknown. Complete absence of one organ of a bilateral pair--absence asymmetry--is rarely found in any animal clade and among insects is otherwise only known for testes in the minute-sized beetles of the family Ptiliidae, ovaries in Scarabaeinae dung beetles, and ovaries of some aphids. Based on current phylogenetic hypotheses for Carabidae, testis loss has occurred independently at least three times, and up to five origins are possible, given the variation within Abacetini. Clear phylogenetic evidence for multiple independent origins suggests an adaptive or functional cause for this asymmetry. A previously posited taxon-specific hypothesis wherein herbivory in the tribe Harpalini led to testis loss is rejected. Optimal visceral packing of the beetle abdomen is suggested as a general explanation. Specifically, based on the function of various organ systems, we hypothesize that interaction of internal organs and pressure to optimize organ size and space usage in each system led to the multiple origins and maintenance of the monorchid condition. Testes are the only redundant and symmetrically paired structures not thought to be developmentally linked to other symmetrical structures in the abdomen. Among all possible organs, they are the most likely--although the observed frequency is very small--to bypass constraints that maintain bilateral symmetry, resulting in absence asymmetry. However, based solely on our observations of gross morphology of internal organs, no function conclusively explains the ontogenetic loss of one testis in these taxa. Unlike the analogous absence asymmetry of organs in other animal groups, no dramatic body-form constraint--e.g., snakes and lung loss, ptiliid beetles' small body-size and relatively giant sperm--or adaptive scenario of improved locomotory performance--e.g., birds and ovary loss due to flight constraints-applies to these carabid beetles. We tentatively suggest that testis loss is driven wholly by an interaction among the internal organs of these beetles, possibly due to selective pressure to maximize the comparatively large accessory glands found in these taxa. However, as the ordering of these evolutionary events of testis loss and accessory gland size increase is not known, large accessory glands might have secondarily evolved to compensate for a decreased testicular output. Copyright 2005 Wiley-Liss, Inc.

PMID: 15732050 [PubMed - indexed for MEDLINE]