Molecular Evidence for Ancient Asexuality in Timema Stick Insects

Abstract

Asexuality is rare in animals in spite of its apparent advantage relative to sexual reproduction, indicating that it must be associated with profound costs [1-9]. One expectation is that reproductive advantages gained by new asexual lineages will be quickly eroded over time [3, 5-7]. Ancient asexual taxa that have evolved and adapted without sex would be "scandalous" exceptions to this rule, but it is often difficult to exclude the possibility that putative asexuals deploy some form of "cryptic" sex, or have abandoned sex more recently than estimated from divergence times to sexual relatives [10]. Here we provide evidence, from high intraspecific divergence of mitochondrial sequence and nuclear allele divergence patterns, that several independently derived Timema stick-insect lineages have persisted without recombination for more than a million generations. Nuclear alleles in the asexual lineages displayed significantly higher intraindividual divergences than in related sexual species. In addition, within two asexuals, nuclear allele phylogenies suggested the presence of two clades, with sequences from the same individual appearing in both clades. These data strongly support ancient asexuality in Timema and validate the genus as an exceptional opportunity to attack the question of how asexual reproduction can be maintained over long periods of evolutionary time.

The Evolutionary Dynamics of Apomixis in Ferns: A Case Study from Polystichoid Ferns

“…This hypothesis is consistent with reported evidence for shortlived apomictic lineages, for example, the derived fern genus Astrolepis [5], and the developmental feature changes required for the loss of sexuality in plants [3]. However, it is inconsistent with other studies that recover evidence for species rich lineages that lack any reported evidence for at least rare sexual events [6,7], and a recent study on the eudicot genus Oenothera, which shows "increasing diversification associated with loss of sexual recombination and segregation" [4]. This conflicting evidence questions 2 Journal of Botany our general understanding of the evolution of asexual reproduction, and the causes of its uneven distribution among animals and land plants.…”

Meiosis and Its Deviations in Polyploid Animals

“…Animals that are incapable of adapting to changes in their environment are arguably doomed to extinction if major changes occur and would represent evolutionary dead ends [Matthey, 1941;White, 1970White, , 1973. Nevertheless, the ones studied by Matthey and White are currently doing well: some have persisted for hundreds of millions of years, prompting Maynard Smith to label bdelloid rotifers 'evolutionary scandals' [Schön et al, 2009; see also Schwander et al, 2011], or at least tens of thousands of years . Many modes of parthenogenesis allow the retention of new mutations and genetic variation.…”

Neutral and selection-driven decay of sexual traits in asexual stick insects

“…Finally, the development of functional males may indicate that lineages presumed to be asexual have some low level of cryptic sex. However, although formally demonstrating the lack of sexual reproduction in a lineage is challenging [53], this explanation is unlikely in groups that display the genomic signatures of asexuality, such as Timema [25,30,54], and is difficult to reconcile with decay of sexual traits in females, reported in cases with functional males [37] (this study).…”

“…For each of the five sexual species, we conducted 109 -211 trials (30-98 for each of the three female groups), for a total of 751 two-choice trials, with different individuals used Table 1. Independently derived asexual Timema lineages and their sexual sister species, ranked by increasing upper age estimates (age estimates from [25], based on intra-and interspecific molecular divergences). The asexual lineages in bold were included in this study.…”

“…Here, we investigate the fate of a suite of sexual traits, including male-specific traits, in five independently derived asexual stick insects in the genus Timema. Because the transitions from sexual reproduction to asexuality have occurred at different times in these lineages (some lineages are recently derived asexuals while others have been asexual for over one million years [24,25]), a temporal component can be included, with a higher level of sexual trait decay expected in old when compared with young asexual lineages. Our results show that neutral traits display little or no regression even in old asexuals, whereas ( presumably) selected traits display major shifts already in young asexuals, such that reversals to sexual reproduction are unlikely, even for recently derived asexual lineages.…”