Evolutionary dynamics of specialisation in herbivorous stick insects.

Understanding the evolutionary dynamics underlying herbivorous insect mega-diversity requires investigating the ability of insects to shift and adapt to different host plants. Feeding experiments with nine related stick insect species revealed that insects retain the ability to use ancestral host plants after shifting to novel hosts, with host plant shifts generating fundamental feeding niche expansions. These expansions were, however, not accompanied by expansions of the realised feeding niches, as species on novel hosts are generally ecologically specialised. For shifts from angiosperm to chemically challenging conifer hosts, generalist fundamental feeding niches even evolved jointly with strong host plant specialisation, indicating that host plant specialisation is not driven by constraints imposed by plant chemistry. By coupling analyses of plant chemical compounds, fundamental and ecological feeding niches in multiple insect species, we provide novel insights into the evolutionary dynamics of host range expansion and contraction in herbivorous insects.

Fundamental and realized feeding niche breadths of sexual and asexual stick insects.

The factors contributing to the maintenance of sex over asexuality in natural populations remain unclear. Ecological divergences between sexual and asexual lineages could help to maintain reproductive polymorphisms, at least transiently, but the consequences of asexuality for the evolution of ecological niches are unknown. Here, we investigated how niche breadths change in transitions from sexual reproduction to asexuality. We used host plant ranges as a proxy to compare the realized feeding niche breadths of five independently derived asexual Timema stick insect species and their sexual relatives at both the species and population levels. Asexual species had systematically narrower realized niches than sexual species, though this pattern was not apparent at the population level. To investigate how the narrower realized niches of asexual species arise, we performed feeding experiments to estimate fundamental niche breadths but found no systematic differences between reproductive modes. The narrow realized niches found in asexual species are therefore probably a consequence of biotic interactions such as predation or competition, that constrain realized niche size in asexuals more strongly than in sexuals.

Nematode endoparasites do not codiversify with their stick insect hosts.

Host-parasite coevolution stems from reciprocal selection on host resistance and parasite infectivity, and can generate some of the strongest selective pressures known in nature. It is widely seen as a major driver of diversification, the most extreme case being parallel speciation in hosts and their associated parasites. Here, we report on endoparasitic nematodes, most likely members of the mermithid family, infecting different Timema stick insect species throughout California. The nematodes develop in the hemolymph of their insect host and kill it upon emergence, completely impeding host reproduction. Given the direct exposure of the endoparasites to the host's immune system in the hemolymph, and the consequences of infection on host fitness, we predicted that divergence among hosts may drive parallel divergence in the endoparasites. Our phylogenetic analyses suggested the presence of two differentiated endoparasite lineages. However, independently of whether the two lineages were considered separately or jointly, we found a complete lack of codivergence between the endoparasitic nematodes and their hosts in spite of extensive genetic variation among hosts and among parasites. Instead, there was strong isolation by distance among the endoparasitic nematodes, indicating that geography plays a more important role than host-related adaptations in driving parasite diversification in this system. The accumulating evidence for lack of codiversification between parasites and their hosts at macroevolutionary scales contrasts with the overwhelming evidence for coevolution within populations, and calls for studies linking micro- versus macroevolutionary dynamics in host-parasite interactions.

Genetic control of contagious asexuality in the pea aphid.

Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼ 300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages.