Sexual conflict in action: An antagonistic relationship between maternal and paternal sex allocation in the tammar wallaby, Notamacropus eugenii

Abstract

Sex ratio biases are often inconsistent, both among and within species and populations. While some of these inconsistencies may be due to experimental design, much of the variation remains inexplicable. Recent research suggests that an exclusive focus on mothers may account for some of the inconsistency, with an increasing number of studies showing variation in sperm sex ratios and seminal fluids. Using fluorescent in‐situ hybridization, we show a significant population‐level Y‐chromosome bias in the spermatozoa of wild tammar wallabies, but with significant intraindividual variation between males. We also show a population‐level birth sex ratio trend in the same direction toward male offspring, but a weaning sex ratio that is significantly female‐biased, indicating that males are disproportionately lost during lactation. We hypothesize that sexual conflict between parents may cause mothers to adjust offspring sex ratios after birth, through abandonment of male pouch young and reactivation of diapaused embryos. Further research is required in a captive, controlled setting to understand what is driving and mechanistically controlling sperm sex ratio and offspring sex ratio biases and to understand the sexually antagonistic relationship between mothers and fathers over offspring sex. These results extend beyond sex allocation, as they question studies of population processes that assume equal input of sex chromosomes from fathers, and will also assist with future reproduction studies for management and conservation of marsupials.

Parental effects on offspring sex ratio in the Numbat (Myrmecobius fasciatus): does captivity influence paternal sex allocation?

“…Studies on disparate mammal species, including the Pygmy Hippopotamus (Choeropsis liberiensis; Saragusty et al 2012), the Whitefooted Deermouse (Peromyscus leucopus; Malo et al 2017), and another Australian marsupial, the Tammar Wallaby (Notamacropus eugenii; Edwards et al 2019), have implicated fathers to be arbiters of sex allocation by reporting positive correlations between sperm (i.e., proportion of X-to y-CBS) and offspring sex ratios. Specifically, the tammar wallaby study reported a population-level bias in both the production of y-CBS and the birth of sons (Edwards et al 2019).…”

Males can adjust offspring sex ratio in an adaptive fashion through different mechanisms

“…Sperm SRs can also differ between males. [29,30,32] Although variance in a trait is a prerequisite for selection, a fair amount of the interindividual variation in sperm SR may be caused by random processes that do not contribute to selection. Three studies have played a major role in elucidating the drivers of this variation.…”

“…Some authors have suggested that a population-level comparison of sperm SR and SR at birth (or inde-pendence) allows sexual conflicts between fathers and mothers over offspring SRs to be examined. Thus, Edwards et al [30] showed a population-level sperm SR biased towards Y-CBS (51.1%) but a weaning SR that is female-biased (80%) in an article entitled "Sexual conflict in action: an antagonistic relationship between maternal and paternal sex allocation in the tammar wallaby". Unfortunately, these conclusions are questionable for two reasons.…”

“…Several recent studies have found unequal numbers of male and female sperm cells in ejaculates (Figure 2). The two represented taxons are mammals, [ 29–32 ] in which spermatozoa contain either an X or Y chromosome (the XY system), and spiders, [ 33 ] in which spermatozoa contain either an X chromosome or no sex chromosome (the X0 system). In both cases, females are the homogametic sex (XX).…”

“…Thus, Edwards et al. [ 30 ] showed a population‐level sperm SR biased towards Y‐CBS (51.1%) but a weaning SR that is female‐biased (80%) in an article entitled “Sexual conflict in action: an antagonistic relationship between maternal and paternal sex allocation in the tammar wallaby”. Unfortunately, these conclusions are questionable for two reasons.…”