Reproductive Versatility of Kelps in Changing Oceans

Abstract

Kelp forests underpin enormous ecological, economic, and cultural values on temperate reefs globally, yet are declining in many places (Krumhansl et al. 2016). Among the most prevalent cause of decline is climate-induced thermal stress, which is resulting in loss and range contractions for many kelp species (e.g., Verg es et al. 2016, Wernberg et al. 2016, Arafeh-Dalmau et al. 2019). While we have an emerging understanding of how these events impact the macroscopic sporophyte stage, knowledge of how gametophytes perform under heat stress and how this varies across their range is scant (Harley et al. 2012, Muth et al. 2019) despite this stage being critical to kelp persistence. One of the primary drivers of performance of natural populations under stress is genetic diversity (Wernberg et al. 2018), which is partly mediated by reproductive traits such as inbreeding. Inbreeding can result in reduced genetic diversity, adaptive capacity, and fitness. As such, many organisms have evolved mechanisms to avoid mating with related individuals. Studies on inbreeding in kelp have revealed that inbreeding is common among natural kelp populations (e.g., Barner et al. 2011, Coleman et al. 2011b) and subsequent fitness effects can be negative (Raimondi et al. 2004) or absent (Barner et al. 2011). However, our understanding of the prevalence, mechanisms, and consequences of inbreeding in kelp remains scant, despite being critical to understanding how kelps might respond and adapt in future oceans. Camus et al. (2021) ambitiously tackle these questions across an unprecedented spatial scale for the giant kelp, Macrocystis pyrifera, to unravel the influence of kinship on kelp performance. The authors conduct gametophyte crossing experiments simulating full inbreeding (parthenogenesis), selfing, and outbreeding (interand intra-population crosses) and measured the consequences for gametophyte morphology, fecundity, and fertility. The authors found that while fully inbred and selfed gametophytes were larger and had more and bigger oogonia than outbred individuals, they had lower fertility resulting in the production of fewer embryos relative to outbred gametophytes. In contrast, outbred gametophytes continued to produce oogonia over a longer period and were subsequently all fertilized. This compensatory mechanism meant that reproductive output was similar regardless of the level of inbreeding. Interestingly, these effects were apparent prior to sexual contact suggesting that females can sense the presence and identity of males and consequently change their morphology and fecundity (Fig. 1). While the mechanisms facilitating this are unknown, the authors suggest that females might sense males through a combination of chemicals released by the male gametophyte or through their microbiomes. Regardless, the putative ability of females to sense appropriate males with which to reproduce is a novel finding that may provide a competitive advantage in warming oceans where sex ratios can be skewed (Fig. 1; Oppliger et al. 2011, Wood et al. 2021). Taking a step further, the authors examined the fitness of the subsequent sporophyte generation, finding little evidence of negative fitness consequences associated with inbreeding. There were few differences in sporophyte morphological traits and no effect of a marine heatwave among breeding treatments. Only holdfast size was smaller in inbred individuals, but the fitness consequences of this single morphological trait are unknown. While similar to results found by Barner et al. (2011), the finding of no inbreeding depression differs from previous modeling (Johansson et al. 2013) and field (Raimondi et al 2004) studies. These differing results between modeling, laboratory, and field studies emphasize the need for more research in this area, particularly multigenerational studies that span life stages. Moreover, mortality in the heatwave treatment was high (80–90%) regardless of inbreeding treatment suggesting that this magnitude of temperature anomaly exceeded any inherent genetic ability to tolerate heat stress. The implications of more J. Phycol. 57, 708–710 (2021) © 2021 Phycological Society of America DOI: 10.1111/jpy.13171