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Male sexual signaling and expected effects of hatchery-induced sperm competition vary with water depth at which whitefish are caught

Wedekind, Claus1; Perroud, Giulia1; Nusbaumer, David1; de Guttry, Christian1

Published Jul 12, 2023 on Dryad. https://doi.org/10.5061/dryad.k6djh9wc9

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Jul 12, 2023 version files 17.55 KB

Abstract

Salmonids like whitefish (Coregonus spp.) are often propagated in supportive breeding. Spawners are caught from their spawning locations, their gametes mixed, and the resulting offspring reared in a protected environment before being released into the wild. This procedure can affect sexual selection, for example, by enhancing the importance of sperm competition or by reducing the relevance of sexual signals. While it is often unclear how sperm competitiveness is affected by a male’s overall genetic quality, there is accumulating evidence that sexual signals reveal good genes and that mate choice based on such signals can increase offspring viability (Auld et al. 2019). Therefore, supportive breeding may affect the genetic variance and the mean genetic quality of next generations. We sampled whitefish from various locations along a depth gradient to test how male characteristics that are likely to affect sexual selection under natural conditions correlate with characteristics that affect hatchery-induced sperm competition. Whitefish are external fertilizers, and multi-male spawning and hence sperm competition is common under natural conditions. Mate choice is not sufficiently understood but could be based on breeding tubercles. These are small conical structures that grow on scales before the breeding sea- son and fall off shortly afterwards. The size of breeding tubercles varies much among males and has repeatedly been found to correlate positively with offspring viability (Wedekind et al. 2001; Keka ̈la ̈inen et al. 2010). Male dominance is typically depend- ent on body size (Auld et al. 2019) and could also be relevant in whitefish. Body size itself can reflect individual inbreeding coefficients (Su et al. 1996) and be an indicator of heritable genetic quality in small or structured populations (Neff and Pitcher 2008). In another fish with a somewhat comparable mating system, the size of breeding tubercles and male size was not correlated but could both be used to predict male reproductive success under close to natural conditions (Jacob et al. 2009). We study whitefish from Lake Hallwil (Switzerland). This lake has suffered so much from anthropogenic eutrophication that it is being artificially aerated since 1985. Three hatcheries around the lake are likely to have played a key role in maintaining the whitefish population, as concluded also from a recent mark–recapture experiment (Vonlanthen 2015). However, eutrophication combined with possible hybridization in hatcheries can have led to a speciation reversal (Vonlanthen et al. 2012) and may thereby have destroyed any genetic structure linked to water depth. Hatchery protocols now focus on maintaining over-all genetic variance by pooling milt of many males before adding the mix to eggs of multiple females. Milt volume varies among sires, for example, because males often lose milt when being pulled up from deep locations (Figure 1), an effect that likely depends on how much the swim bladder is inflated by the change in pressure. This variance in milt volume is likely to affect the genetic variance that, in combination with the average genetic quality, may then affect the long-term survival of a population. The extent to which hatchery protocols affect genetic quality can be estimated by the correlations between male quality indicators and traits that affect hatchery-induced sperm competition, that is, sperm number, velocity, and longevity (summarized here as “milt potency,” see also Supplementary Material). Many breeding protocols are likely to promote genetic quality if male attractiveness or dominance are positively correlated to milt potency. If there are no such correlations or negative ones because of life-history trade-offs, hatchery-induced sperm competition is likely to reduce the average genetic quality in future generations. We sampled fish from various depths and determined their age, size, breeding ornamentation, and milt potency (see methods in the Supplementary Material) to test whether and how different male characteristics affect reproductive success in supportive breeding in a heavily managed population.