Łukasz Michalczyk

Inbreeding Promotes Female Promiscuity

After a population bottleneck, polyandry allows females to select sperm with the best prospects for fitness. The widespread phenomenon of polyandry (mating by females with multiple males) is an evolutionary puzzle, because females can sustain costs from promiscuity, whereas full fertility can be provided by a single male. Using the red flour beetle, Tribolium castaneum, we identify major fitness benefits of polyandry to females under inbreeding, when the risks of fertilization by incompatible male haplotypes are especially high. Fifteen generations after inbred populations had passed through genetic bottlenecks, we recorded increased levels of female promiscuity compared with noninbred controls, most likely due to selection from prospective fitness gains through polyandry. These data illustrate how this common mating pattern can evolve if population genetic bottlenecks increase the risks of fitness depression due to fertilization by sperm carrying genetically incompatible haplotypes.

META-ANALYSIS SUGGESTS CHOOSY FEMALES GET SEXY SONS MORE THAN “GOOD GENES”

Female preferences for specific male phenotypes have been documented across a wide range of animal taxa, including numerous species where males contribute only gametes to offspring production. Yet, selective pressures maintaining such preferences are among the major unknowns of evolutionary biology. Theoretical studies suggest that preferences can evolve if they confer genetic benefits in terms of increased attractiveness of sons (“Fisherian” models) or overall fitness of offspring (“good genes” models). These two types of models predict, respectively, that male attractiveness is heritable and genetically correlated with fitness. In this meta‐analysis, we draw general conclusions from over two decades worth of empirical studies testing these predictions (90 studies on 55 species in total). We found evidence for heritability of male attractiveness. However, attractiveness showed no association with traits directly associated with fitness (life‐history traits). Interestingly, it did show a positive correlation with physiological traits, which include immunocompetence and condition. In conclusion, our results support “Fisherian” models of preference evolution, while providing equivocal evidence for “good genes.” We pinpoint research directions that should stimulate progress in our understanding of the evolution of female choice.

Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum

As populations decline to levels where reproduction among close genetic relatives becomes more probable, subsequent increases in homozygous recessive deleterious expression and/or loss of heterozygote advantage can lead to inbreeding depression. Here, we measure how inbreeding across replicate lines of the flour beetle Tribolium castaneum impacts on male reproductive fitness in the absence or presence of male–male competition. Effects on male evolution from mating pattern were removed by enforcing monogamous mating throughout. After inbreeding across eight generations, we found that male fertility in the absence of competition was unaffected. However, we found significant inbreeding depression of sperm competitiveness: non-inbred males won 57 per cent of fertilizations in competition, while inbred equivalents only sired 42 per cent. We also found that the P2 ‘offence’ role in sperm competition was significantly more depressed under inbreeding than sperm ‘defence’ (P1). Mating behaviour did not explain these differences, and there was no difference in the viability of offspring sired by inbred or non-inbred males. Sperm length variation was significantly greater in the ejaculates of inbred males. Our results show that male ability to achieve normal fertilization success was not depressed under strong inbreeding, but that inbreeding depression in these traits occurred when conditions of sperm competition were generated.

EXPERIMENTAL EVOLUTION EXPOSES FEMALE AND MALE RESPONSES TO SEXUAL SELECTION AND CONFLICT IN TRIBOLIUM CASTANEUM

Between‐individual variance in potential reproductive rate theoretically creates a load in reproducing populations by driving sexual selection of male traits for winning competitions, and female traits for resisting the costs of multiple mating. Here, using replicated experimental evolution under divergent operational sex ratios (OSR, 9:1 or 1:6 ♀:♂) we empirically identified the parallel reproductive fitness consequences for females and males in the promiscuous flour beetle Tribolium castaneum. Our results revealed clear evidence that sexual conflict resides within the T. castaneum mating system. After 20 generations of selection, females from female‐biased OSRs became vulnerable to multiple mating, and showed a steep decrease in reproductive fitness with an increasing number of control males. In contrast, females from male‐biased OSRs showed no change in reproductive fitness, irrespective of male numbers. The divergence in reproductive output was not explained by variation in female mortality. Parallel assays revealed that males also responded to experimental evolution: individuals from male‐biased OSRs obtained 27% greater reproductive success across 7‐day competition for females with a control male rival, compared to males from the female‐biased lines. Subsequent assays suggest that these differences were not due to postcopulatory sperm competitiveness, but to precopulatory/copulatory competitive male mating behavior.

Sexual selection protects against extinction

Reproduction through sex carries substantial costs, mainly because only half of sexual adults produce offspring. It has been theorized that these costs could be countered if sex allows sexual selection to clear the universal fitness constraint of mutation load. Under sexual selection, competition between (usually) males and mate choice by (usually) females create important intraspecific filters for reproductive success, so that only a subset of males gains paternity. If reproductive success under sexual selection is dependent on individual condition, which is contingent to mutation load, then sexually selected filtering through ‘genic capture’ could offset the costs of sex because it provides genetic benefits to populations. Here we test this theory experimentally by comparing whether populations with histories of strong versus weak sexual selection purge mutation load and resist extinction differently. After evolving replicate populations of the flour beetle Tribolium castaneum for 6 to 7 years under conditions that differed solely in the strengths of sexual selection, we revealed mutation load using inbreeding. Lineages from populations that had previously experienced strong sexual selection were resilient to extinction and maintained fitness under inbreeding, with some families continuing to survive after 20 generations of sib × sib mating. By contrast, lineages derived from populations that experienced weak or non-existent sexual selection showed rapid fitness declines under inbreeding, and all were extinct after generation 10. Multiple mutations across the genome with individually small effects can be difficult to clear, yet sum to a significant fitness load; our findings reveal that sexual selection reduces this load, improving population viability in the face of genetic stress.

Age dependence of male mating ability and sperm competition success in the bulb mite

In many species, the genetic quality of gametes is likely to decline with age of the male. Some form of discrimination against mating with old males, or against fertilization by their sperm, can be expected to evolve. We investigated the effect of male age on the probability of mating and on sperm competitiveness in the bulb mite, Rhizoglyphus robini. There was no significant difference between male age classes in the probability of mating with virgin females, but young males were more likely to mate with already mated females. Furthermore, young males won sperm competition against older males. This implies that polyandry may be an effective way of avoiding fertilization by the sperm of older males. It has also been suggested that polyandry insures females against the infertility of old males. Our results do not support this hypothesis: matings with older males did not result in female infertility significantly more often than matings with young males.

Annotated zoogeography of non-marine Tardigrada

This paper is the second monograph of nine that describes the global records of limno-terrestrial water bears (Tardigrada). Here, we provide a comprehensive list of non-marine tardigrades recorded from South America, providing an updated and revised taxonomy accompanied by geographic co-ordinates, habitat, and biogeographic comments. It is hoped this work will serve as a reference point and background for further zoogeographical and taxonomical studies.

Annotated zoogeography of non-marine Tardigrada. Part I: Central America.

Dividing the world into nine regions, this first paper describes literature records of the limno-terrestrial tardigrades (Tardigrada) reported from Central America. Updating previously published species lists we have revised the taxonomy and provided additional habitat, geographic co-ordinates, and biogeographic comments. It is hoped this work will serve as a reference point and background for further zoogeographic studies.

Tardigrada of the Revdalen (Spitsbergen) with the descriptions of two new species: Bryodelphax parvuspolaris (Heterotardigrada) and Isohypsibius coulsoni (Eutardigrada)

Despite a century long history of research, tardigrade fauna of the Svalbard Archipelago remains poorly known. In order to deepen our knowledge of tardigrade biodiversity in the Arctic, we collected forty-one moss and lichen samples from the Revdalen and on the south-east slopes of the Rotjesfjellet (Spitsbergen, Svalbard Archipelago) in June 2010. In these samples, twenty-five tardigrade species were found, including two new for science: Bryodelphax parvuspolaris sp. nov. and Isohypsibius coulsoni sp. nov. B. parvuspolaris sp. nov. belongs to the weglarskae group but differs from all other species of the group by a unique configuration of ventral plates. I. coulsoni sp. nov. differs from the most similar species I. ceciliae Pilato and Binda, 1987 mainly by the absence of ventral sculpture. Two additional species, Milnesium asiaticum Tumanov, 2006 and Diphascon (Adropion) prorsirostre Thulin, 1928, are recorded from the Svalbard Archipelago for the first time.

An integrative description of Macrobiotus paulinae sp. nov. (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group) from Kenya.

In this paper we describe Macrobiotus paulinae, a new species of the hufelandi group from the Kenyan highlands. In addition to the traditional taxonomic description, aided with morphometrics as well as light and scanning microscopy imaging, we also provide nucleotide sequences of three nuclear (18S rRNA, 28S rRNA, ITS-2) and one mitochondrial (COI) DNA fragment of the new species. The sequences allowed not only a more accurate description but also provided an independent verification of the taxonomic status of Ma. paulinae sp. nov. Such integrative approach requires a considerable number of individuals and eggs, which we have partially subsidised by employing an in vitro culture of the new species. Our analyses revealed that Ma. paulinae sp. nov. is most similar to Macrobiotus madegassus Maucci, 1993 and Macrobiotus modestus Pilato & Lisi, 2009, however it differs from these species, as well as from all other known species of the hufelandi group, by the presence of seven paired dorso-lateral patches of cuticular granulation and the presence of chorionic filaments growing out of terminal discs of egg processes. Macrobiotus paulinae sp. nov. is an example of a species with a miniaturised buccal apparatus (i.e. with reduced peribuccal lamellae and oral cavity armature, and stylet supports inserted on the buccal tube more anteriorly than in typical Ma. hufelandi group species), and it therefore resembles two recently described two-macroplacoided Minibiotus species: Mi. acadianus Meyer & Domingue, 2011 and Mi. julianae Meyer, 2012. The re-examination of the type material for these two species confirmed that they are equipped with peribuccal lamellae and therefore we transfer them to the genus Macrobiotus, specifically to the hufelandi group.