Senescence evolution under the catastrophic accumulation of deleterious mutations.

For aging to evolve, selection against mortality must decrease with age. This prevailing view in the evolutionary theory of senescence posits that mutations with deleterious effects happening late in life-when purging selection is weak-may become fixed via genetic drift in the germline, and produce a senescent phenotype. Theory, however, has focused primarily on growing populations and the fate of single deleterious mutations. In a mathematical model, we demonstrate that relaxing both of these simplifying assumptions leads to unrealistic outcomes. In density-regulated populations, previously fixed deleterious mutations should promote the fixation of other deleterious mutations that lead to senescence at ever younger ages, until death necessarily occurs at sexual maturity. This sequential fixation of deleterious mutations is not promoted by a decrease in population size, but is due to a change in the strength of selection. In an individual-based model, we also show that such evolutionary dynamics should lead to the extinction of most populations. Our models therefore make rather unrealistic predictions, underlining the need for a reappraisal of current theories. In this respect, we have further assumed in our models that the deleterious effects of mutations can only occur at certain ages, marked, for instance, by somatic or physiological changes. Under this condition, we show that the catastrophic accumulation of deleterious mutations in the germline can stop. This new finding emphasizes the importance of investigating somatic factors, as well as other mechanisms underlying the deleterious effects of mutations, to understand senescence evolution. More generally, our model therefore establishes that patterns of senescence in nature depend not only on the decrease in selection strength with age but also on any mechanism that stops the catastrophic accumulation of mutations.

Behavioural responses of breeding arctic sandpipers to ground-surface temperature and primary productivity.

Most birds incubate their eggs, which requires time and energy at the expense of other activities. Birds generally have two incubation strategies: biparental where both mates cooperate in incubating eggs, and uniparental where a single parent incubates. In harsh and unpredictable environments, incubation is challenging due to high energetic demands and variable resource availability. We studied the relationships between the incubation behaviour of sandpipers (genus Calidris) and two environmental variables: temperature and a proxy of primary productivity (i.e. NDVI). We investigated how these relationships vary between incubation strategies and across species among strategies. We also studied how the relationship between current temperature and incubation behaviour varies with previous day's temperature. We monitored the incubation behaviour of nine sandpiper species using thermologgers at 15 arctic sites between 2016 and 2019. We also used thermologgers to record the ground surface temperature at conspecific nest sites and extracted NDVI values from a remote sensing product. We found no relationship between either environmental variables and biparental incubation behaviour. Conversely, as ground-surface temperature increased, uniparental species decreased total duration of recesses (TDR) and mean duration of recesses (MDR), but increased number of recesses (NR). Moreover, small species showed stronger relationships with ground-surface temperature than large species. When all uniparental species were combined, an increase in NDVI was correlated with higher mean duration, total duration and number of recesses, but relationships varied widely across species. Finally, some uniparental species showed a lag effect with a higher nest attentiveness after a warm day while more recesses occurred after a cold day than was predicted based on current temperatures. We demonstrate the complex interplay between shorebird incubation strategies, incubation behaviour, and environmental conditions. Understanding how species respond to changes in their environment during incubation helps predict their future reproductive success.

Fluctuating Dynamics of Mate Availability Promote the Evolution of Flexible Choosiness in Both Sexes.

AbstractThe evolution of choosiness has a strong effect on sexual selection, as it promotes variance in mating success among individuals. The context in which choosiness is expressed, and therefore the associated gain and cost, is highly variable. An overlooked mechanism by current models is the rapid fluctuations in the availability and quality of partners, which generates a dynamic mating market to which each individual must optimally respond. We argue that the rapid fluctuations of the mating market are central to the evolution of optimal choosiness. Using a dynamic game approach, we investigate this hypothesis for various mating systems (characterized by different adult sex ratio and latency period combinations), allowing feedback between the choosiness and partner availability throughout a breeding season while taking into account the fine variation in individual quality. Our results indicate that quality-dependent and flexible choosiness usually evolve in both sexes for various mating systems and that a significant amount of variance in choosiness is observed, especially in males, even when courtship is costly. Accounting for the fluctuating dynamics of the mating market therefore allows envisioning a much wider range of choosiness variation in natural populations and may explain a number of recent empirical results regarding choosiness in the less common sex or its variance within sexes.

Transmissible cancers and the evolution of sex under the Red Queen hypothesis.

The predominance of sexual reproduction in eukaryotes remains paradoxical in evolutionary theory. Of the hypotheses proposed to resolve this paradox, the 'Red Queen hypothesis' emphasises the potential of antagonistic interactions to cause fluctuating selection, which favours the evolution and maintenance of sex. Whereas empirical and theoretical developments have focused on host-parasite interactions, the premises of the Red Queen theory apply equally well to any type of antagonistic interactions. Recently, it has been suggested that early multicellular organisms with basic anticancer defences were presumably plagued by antagonistic interactions with transmissible cancers and that this could have played a pivotal role in the evolution of sex. Here, we dissect this argument using a population genetic model. One fundamental aspect distinguishing transmissible cancers from other parasites is the continual production of cancerous cell lines from hosts' own tissues. We show that this influx dampens fluctuating selection and therefore makes the evolution of sex more difficult than in standard Red Queen models. Although coevolutionary cycling can remain sufficient to select for sex under some parameter regions of our model, we show that the size of those regions shrinks once we account for epidemiological constraints. Altogether, our results suggest that horizontal transmission of cancerous cells is unlikely to cause fluctuating selection favouring sexual reproduction. Nonetheless, we confirm that vertical transmission of cancerous cells can promote the evolution of sex through a separate mechanism, known as similarity selection, that does not depend on coevolutionary fluctuations.

Acanthocephalan infection patterns in amphipods: a reappraisal in the light of recently discovered host cryptic diversity.

Amphipods are model species in studies of pervasive biological patterns such as sexual selection, size assortative pairing and parasite infection patterns. Cryptic diversity (i.e. morphologically identical but genetically divergent lineages) has recently been detected in several species. Potential effects of such hidden diversity on biological patterns remain unclear, but potentially significant, and beg the question of whether we have missed part of the picture by involuntarily overlooking the occurrence and effects of cryptic diversity on biological patterns documented by previous studies. Here we tested for potential effects of cryptic diversity on parasite infection patterns in amphipod populations and discuss the implications of our results in the context of previously documented host-parasite infection patterns, especially amphipod-acanthocephalan associations. We assessed infection levels (prevalence and abundance) of 3 acanthocephalan species (Pomphorhynchus laevis, P. tereticollis and Polymorphus minutus) among cryptic lineages of the Gammarus pulex/G. fossarum species complex and G. roeseli from sampling sites where they occur in sympatry. We also evaluated potential differences in parasite-induced mortality among host molecular operational taxonomic units (MOTUs)-parasite species combinations. Acanthocephalan prevalence, abundance and parasite-induced mortality varied widely among cryptic MOTUs and parasite species; infection patterns were more variable among MOTUs than sampling sites. Overall, cryptic diversity in amphipods strongly influenced apparent infection levels and parasite-induced mortality. Future research on species with cryptic diversity should account for potential effects on documented biological patterns. Results from previous studies may also need to be reassessed in light of cryptic diversity and its pervasive effects.

Variations in infection levels and parasite-induced mortality among sympatric cryptic lineages of native amphipods and a congeneric invasive species: Are native hosts always losing?

Shared parasites can strongly influence the outcome of competition between congeneric, sympatric hosts, and thus host population dynamics. Parasite-mediated competition is commonly hypothesized as an important factor in biological invasion success; invasive species often experience lower infection levels and/or parasite-induced mortality than native congeneric hosts. However, variation in infection levels among sympatric hosts can be due to contrasting abilities to avoid infection or different parasite-induced mortality rates following infection. Low parasite infection levels in a specific host can be due to either factor but have drastically different implications in interaction outcomes between sympatric hosts. We assessed acanthocephalan infection levels (prevalence and abundance) among cryptic molecular taxonomic units (MOTU) of the native G. pulex/G. fossarum species complex from multiple populations where they occur in sympatry. We concomitantly estimated the same parameters in the invasive Gammarus roeseli commonly found in sympatry with G. pulex/G. fossarum MOTUs. We then tested for potential differences in parasite-induced mortality among these alternative hosts. As expected, the invasive G. roeseli showed relatively low infection level and was not subject to parasite-induced mortality. We also found that both acanthocephalan infection levels and parasite-induced mortality varied greatly among cryptic MOTUs of the native amphipods. Contrary to expectations, some native MOTUs displayed levels of resistance to their local parasites similar to those observed in the invasive G. roeseli. Overall, cryptic diversity in native amphipods coupled with high levels of variability in infection levels and parasite-induced mortality documented here may strongly influence inter-MOTU interactions and native population dynamics as well as invasion success and population dynamics of the congeneric invasive G. roeseli.

Pairing success and sperm reserve of male Gammarus pulex infected by Cyathocephalus truncatus (Cestoda: Spathebothriidea).

Manipulative parasites with complex life cycles are known to induce behavioural and physiological changes in their intermediate hosts. Cyathocephalus truncatus is a manipulative parasite which infects Gammarus pulex as intermediate host. G. pulex males display pre-copulatory mate guarding as a response to male-male competition for access to receptive females. In this paper, we tested the influence that C. truncatus-infection might have on male G. pulex sperm number and pairing success. We considered 3 classes of G. pulex males in our experiments: (i) uninfected males found paired in the field, (ii) uninfected males found unpaired in the field, or (iii) infected males found unpaired in the field. Both infected males and uninfected unpaired males paired less with a new female than uninfected paired males did. Furthermore, infected males appear to be at a strong disadvantage when directly competing for females with a healthy rival male, and had fewer sperm in their testes. We discuss the potential effect of male and female mating strategies on such male host mating alteration.

Does foreplay matter? Gammarus pulex females may benefit from long-lasting precopulatory mate guarding.

Precopulatory mate guarding (PCMG) is generally assumed to be costly for both sexes. However, males may gain by displaying long-lasting mate guarding under strong male-male competition. Surprisingly, the potential for females to benefit from being held by males has been largely overlooked in previous studies. In Gammarus pulex, an amphipod crustacean, PCMG lasts several weeks, yet females are described as bearing only cost from such male mating strategy. We investigated potential female benefits by assessing the effect of mate guarding on her intermoult duration. Unpaired females had longer intermoult duration than paired females. Intermoult duration clearly decreased when paired females engaged in early and long-lasting mate guarding. In addition, short intermoults and long-lasting mate guarding had no effect on egg number. These results highlight a potential benefit associated with PCMG for G. pulex females, suggesting that the strength of an intersexual conflict over its duration may be overestimated.