Parental feeding preferences rather than sibling competition determine the death of smaller nestlings in asynchronous broods

Hatching asynchrony is a reproductive tactic that, through the creation of competitive hierarchies among offspring, allows parents for a quick adjustment of brood size via the death of smaller nestlings. This strategy is considered to be adaptive in case of unpredictable and/or poor environments in which it would guarantee that at least larger nestlings will fledge. Brood reduction is the usual outcome in asynchronously hatched broods since first-hatched nestlings are larger and get a disproportionately larger share of the food delivered by parents, often leading the youngest nestling to starve to death soon after hatching. However, we still do not know the proximate mechanisms of such brood reduction. One possibility is that the smallest nestling is not fed because larger nestlings outcompete it, which implies that nestlings control resource allocation. Alternatively, parents might actively ignore the persistent begging from their smallest nestling, which would involve that parents control food allocation. To determine whether parents or nestlings ultimately induce brood reduction in this situation, we experimentally created asynchronous broods of Eurasian blackbird (Turdus merula) nestlings and quantified food allocation by parents in two different situations: when sibling competition was allowed and, alternatively, when competition was prevented by physically separating nestlings within the nests by using wooden barriers. Our results showed that experimentally introduced smaller nestlings received less food than their larger nestmates both when competition among nestlings was allowed and when it was prevented. When adult males and females are considered separately, males fed the smallest nestling less often regardless of whether sibling competition was allowed or not, but adult females showed no differences. We can conclude that the smallest nestling starves mainly because parents actively ignore its begging. The higher competitive ability of the larger nestlings seem to have little effect given that although the smallest nestling is fed at a higher rate when physical interactions are prevented by the wooden barrier than when not, this difference is not significant. These findings suggest that parents rather than nestlings have the main control over food allocation.

Hypothesizing novel mating behaviours in the squaretail grouper based on direct behavioural observations

Historically unfished, high-density spawning aggregations are vanishingly uncommon. Behavioural observations from such aggregations are rare, and may be sometimes novel and unexpected. Given the weight of evidence required to document spawning aggregations, how can we best report rare and unusual behavioural variations in spawning populations? Based on two years of in-water observations of a high-density spawning aggregation of the squaretail grouper in the Lakshadweep Archipelago, we described a previously unreported male alternative reproductive tactic (ART) and an inverse size assortment with large males courting several small females that shoaled mid-water (https://doi.org/10.1186/s12898-017-0120-5). In critiquing our manuscript, it has been suggested that our observations, methodologies and interpretation are inadequate, flawed, and do not fit within currently accepted theory (https://doi.org/10.1186/s12898-018-0206-8). While offering a detailed counter of the main methodological and theoretical criticisms we question how best to document and interpret novel behaviours in poorly known systems. Reporting novelty itself can hardly be the basis of criticism. Our report relied on direct in-water observations, conducted at peak densities over two spawning years. The critique ignores this, choosing instead to focus on a supplementary video which was not the basis of our conclusions. Like other researchers working on this species, we did not directly observe mating, but report courtship as a well-established proxy used across mating systems studies. Apart from these methodological concerns, the authors suggest that there is no theoretical support for our observations. However, sexual selection theory provides well-established frameworks showing that, at very high mating densities, a variety of tactics can emerge, that often vary considerably between populations and locations. In our original paper, we use this broader theory of sexual selection together with detailed behavioural data to propose plausible evolutionary explanations that bear testing in these novel, high-density systems. We agree with the authors that novel observations should be scrutinised carefully as they can challenge our current understanding of the range of behaviours populations display and serve as a springboard for theoretical advancement. Given their rarity, these observations should be evaluated against the rigour of their documentation and the transparency of their reporting. In this context, we hope our carefully documented observations serve as a useful addition to the fascinating and complex natural history of species like the squaretail grouper.

Experimental manipulation of reproductive tactics in Seba’s short-tailed bats: consequences on sperm quality and oxidative status

To reproduce, males have to fertilize the female’s eggs, sometimes in competition with ejaculates of other males. In species where males display alternative reproductive tactics, whereby territorial males secure mating and non-territorial males have to sneak copulations, the latter might be expected to invest relatively more resources towards sperm quality compared with the territorial males. Sperm cells are especially vulnerable to oxidative stress, which reduces male fertility. Therefore, antioxidant resources are expected to modulate sperm quality, and might be allocated differently between reproductive tactics. To test the link between reproductive tactics, redox profile and sperm quality, we experimentally induced changes in the reproductive tactics of 39 captive males Seba’s short-tailed bats Carollia perspicillata. We monitored the blood and ejaculate oxidative balance, and the sperm quality before, 7 days and 21 days after the manipulation of reproductive tactic. Although ejaculates’ oxidative damage was negatively related to sperm velocity, males exhibited similar blood and ejaculates redox profiles and similar sperm quality, regardless of their reproductive tactic. Possibly, these results arise as a consequence of some constraints having been lifted during the experiment. Our results also suggest that, in Seba’s short-tailed bats, the expression of alternative reproductive tactics is not subjected to strong oxidative constraints. Furthermore, our results could reflect an absence of trade-off between pre- and post-copulatory traits in harem males, as they could be selected to invest both in female attraction and sperm quality, as a consequence of their inability to fully monopolize females.

The brood parasite's guide to inclusive fitness theory

Hamilton's theory of inclusive fitness provides a framework for understanding the evolution of social behaviour between kin, including parental and alloparental care. Brood parasitism is a reproductive tactic in which parasites exploit the care of other individuals of the same species (conspecific parasitism) or different species (interspecific parasitism) to rear their brood. Here, drawing from examples in birds and social insects, we identify two insights into brood parasitism that stem from inclusive fitness theory. First, the kin structure within nests, or between neighbouring nests, can create a niche space favouring the evolution of conspecific parasitism. For example, low average relatedness within social insect nests can increase selection for reproductive cheats. Likewise, high average relatedness between adjacent nests of some birds can increase a female's tolerance of parasitism by her neighbour. Second, intrabrood conflict will be high in parasitized broods, from the perspective of both parasite and host young, relative to unparasitized broods. We also discuss offspring recognition by hosts as an example of discrimination in a kin-selected social behaviour. We conclude that the inclusive fitness framework is instructive for understanding aspects of brood parasite and host evolution. In turn, brood parasites present some unique opportunities to test the predictions of inclusive fitness theory.This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

Novel mating behaviours in the squaretail grouper: Response to “Fake spawns and floating particles"

Based on two years of in-water observations of a high-density spawning aggregation of the squaretail grouper in the Lakshadweep Archipelago, we described a previously unreported inverse size assortment with large males courting several small females that shoaled mid-water (DOI 10.1186/s12898-017-0120-5). Critiquing our manuscript, Erisman and colleagues (DOI 10.1186/s12898-018-0206-8) suggest that our observations and interpretation are flawed, and do not fit within currently accepted theory. Here we offer a detailed counter of their main methodological and theoretical criticisms. Their criticism that this reproductive tactic has never been observed before is hardly a criticism since its novelty is precisely what we wished to highlight. The supplementary video that Erisman et al use to base much of their criticisms was not the basis of our conclusions, which relied on direct in-water observations. These observations were conducted over two spawning years, taking care to ensure that we sampled aggregations at peak densities. Like other researchers working on this species, we did not directly observe mating, but have used courtship as a proxy for mating success – a well-established proxy across mating systems studies. Apart from these methodological concerns, the authors suggest that there is no theoretical support for our observations. However, sexual selection theory provides a well-established framework showing that, at very high mating densities, a variety of tactics can emerge, that often vary considerably between populations and locations. We agree with the authors that novel observations should be scrutinised carefully. They challenge our current understanding of the range of behaviours populations display and serve as a springboard for theoretical advancement. We stand by our observations and hope they serve as a useful addition to the fascinating and complex natural history of species like the squaretail grouper.

Novel mating behaviours in the squaretail grouper: Response to “Fake spawns and floating particles"

Based on two years of in-water observations of a high-density spawning aggregation of the squaretail grouper in the Lakshadweep Archipelago, we described a previously unreported inverse size assortment with large males courting several small females that shoaled mid-water (DOI 10.1186/s12898-017-0120-5). Critiquing our manuscript, Erisman and colleagues (DOI 10.1186/s12898-018-0206-8) suggest that our observations and interpretation are flawed, and do not fit within currently accepted theory. Here we offer a detailed counter of their main methodological and theoretical criticisms. Their criticism that this reproductive tactic has never been observed before is hardly a criticism since its novelty is precisely what we wished to highlight. The supplementary video that Erisman et al use to base much of their criticisms was not the basis of our conclusions, which relied on direct in-water observations. These observations were conducted over two spawning years, taking care to ensure that we sampled aggregations at peak densities. Like other researchers working on this species, we did not directly observe mating, but have used courtship as a proxy for mating success – a well-established proxy across mating systems studies. Apart from these methodological concerns, the authors suggest that there is no theoretical support for our observations. However, sexual selection theory provides a well-established framework showing that, at very high mating densities, a variety of tactics can emerge, that often vary considerably between populations and locations. We agree with the authors that novel observations should be scrutinised carefully. They challenge our current understanding of the range of behaviours populations display and serve as a springboard for theoretical advancement. We stand by our observations and hope they serve as a useful addition to the fascinating and complex natural history of species like the squaretail grouper.

Condition-dependent female preference for male genitalia length is based on male reproductive tactics

There is extensive morphological variation of male genitalia across animals with internal fertilization, even among closely related species. Most studies attempting to explain this extraordinary diversity have focused on processes that occur post-copula (e.g. sperm competition, cryptic female choice). Only a few studies have focused on the pre-copula process of female preference. In addition, the extent to which this variation could be associated with the use of different reproductive tactics has yet to be explored. Here, we show that female preference for male genitalia length in two livebearing fishes depends on the type of reproductive tactic of the males being evaluated as well as the body condition of the female. In a species where all males coax females to acquire matings (courters), females preferred males with short genitalia. In a species with genetically influenced alternative reproductive tactics (courter males that only court and produce courter sons, sneaker males that use the coercive tactic of sneak chase and produce sneaker sons), female preference depended on an interaction between male tactic and female condition: females in good condition preferred courter males with short genitalia, and sneaker males with long genitalia. Our results suggest that female preference for male traits favourable to their sons may be an important factor contributing to the diversification of male genitalia. Despite the contrasting selection for genitalia length that our female preference tests suggest, we found no significant differences in genitalia length between coaxing (courters) and coercive (sneakers) males. Our study represents a starting point to more clearly understand the role of alternative reproductive tactics and variation in female mate preference in the evolution of male genitalia.