TY - JOUR
AU1 - Schwarz,, Rachel
AU2 - Itescu,, Yuval
AU3 - Antonopoulos,, Antonis
AU4 - Gavriilidi,, Ioanna-Aikaterini
AU5 - Tamar,, Karin
AU6 - Pafilis,, Panayiotis
AU7 - Meiri,, Shai
AB - Abstract Insular animals are thought to be under weak predation pressure and increased intraspecific competition compared with those on the mainland. Thus, insular populations are predicted to evolve ‘slow’ life histories characterized by fewer and smaller clutches of larger eggs, a pattern called the ‘island syndrome’. To test this pattern, we collected data on egg volume, clutch size and laying frequency of 31 Aegean Island populations of the closely related geckos of the Mediodactylus kotschyi species complex. We tested how predation pressure, resource abundance, island area and isolation influenced reproductive traits. Isolation and predation were the main drivers of variation in life-history traits. Higher predator richness seemed to promote faster life histories, perhaps owing to predation on adults, whereas the presence of boas promoted slower life histories, perhaps owing to release from predation by rats on the eggs of geckos. Insular geckos followed only some of the predictions of the ‘island syndrome’. Predation pressure seemed to be more complex than expected and drove life histories of species in two opposing directions. Our results highlight the importance of considering the identity of specific predators in ecological studies. Aegean Islands, clutch frequency, clutch size, egg volume, geckos, island biology, island syndrome, life-history traits Introduction Life-history strategies vary along a continuum that stretches from ‘fast’ life histories (i.e. frequent, large clutches of small hatchlings, ‘r strategy’) to ‘slow’ ones (i.e. infrequent, small clutches of large hatchlings, ‘K strategy’; MacArthur & Wilson, 1967; Pianka, 1970, 2011). Females can either produce larger clutches leading to ‘faster’ life histories (Peters, 1983; Roff, 1992; Honek, 1993; Scharf & Meiri, 2013) or produce few, larger offspring (Roff, 1992; Preziosi et al., 1996) with higher probability of survival, promoting ‘slower’ life histories. They cannot, however, produce both larger clutches and large offspring, because of limitations on the volume available in the females’ abdomens (Pianka, 1970; but see Pafilis et al. 2011). In some taxa, however, increasing the number of eggs in a clutch is not possible (e.g. in geckos and anoles). Such taxa may increase reproductive output by producing larger offspring or by laying more frequently (Schall, 1983; Stearns, 1992; Doughty, 1997; Kratochvil & Frynta, 2006; Ma et al., 2019; but see Shine, 1988). Life-history traits such as clutch (or litter) size and frequency of reproduction, egg volume, hatchling size, growth rates and age at maturity of insular populations have been studied intensively and often differ from those of mainland kin (e.g. Stearns, 1992; Adler & Levins, 1994; Adamopoulou & Valakos, 2000; Goltsman et al., 2005; Huang, 2007; Raia et al., 2010; Pafilis et al., 2011; Monti et al., 2012; Novosolov & Meiri, 2013; Novosolov et al., 2013; Slavenko et al., 2015; Schwarz & Meiri, 2017; Uller et al., 2019). Small, distant islands, harbour fewer predators (MacArthur & Wilson, 1967), facilitating higher survival rates among local inhabitants (Crowell, 1962; MacArthur & Wilson, 1967; MacArthur et al., 1972; Adler & Levins, 1994). These, in turn, facilitate denser populations on islands (‘density compensation’; MacArthur et al., 1972; Rodda & Dean-Bradley, 2002; Novosolov et al., 2016). The ‘island syndrome’, a pattern Adler & Levins (1994) described and named in rodent populations, predicts that insular populations will be denser and more stable and will exhibit higher survival rates, larger body size, reduced aggressiveness and lower reproductive output in comparison to mainland populations. These features are thought to occur mainly as a consequence of lower predation pressure and relaxed interspecific competition on islands compared with the mainland (Adler & Levins, 1994). These differences lead to reduced reproductive effort and overall ‘slower’ life histories on islands (Sinervo et al., 2000; Novosolov & Meiri, 2013), which may include delayed sexual maturity, small clutches of larger offspring (Adler & Levins, 1994) and reduced clutch frequency (Shine, 1988; but see Huang, 2007; Novosolov et al., 2013). Denser populations on islands may lead to stronger intraspecific competition, increasing juvenile mortality through infanticide and cannibalism (Jenssen et al., 1989; Elgar & Crespi, 1992; Pafilis et al., 2009; Cooper et al., 2015). Consequently, selection for large hatchlings, which presumably better avoid predation, might also drive adult body size to increase (Melton, 1982; Pafilis et al., 2009). Insular lizards were found to sustain dense populations, small clutch sizes (but high brood frequencies) and large offspring compared with closely related mainland taxa or populations (Schall, 1983; Buckley & Jetz, 2007; Novosolov et al., 2013; Novosolov & Meiri, 2013; Schwarz & Meiri, 2017), mainly in line with the island syndrome. The Aegean archipelago (Mediterranean Sea, Greece) constitutes a fascinating system for studying trait evolution on islands (Lymberakis et al., 2018). It comprises islands that vary greatly in area, isolation and geological history and that host diverse fauna and flora (Sfenthourakis & Triantis, 2017). Therefore, this archipelago enables a detailed examination of the effects of insularity on the evolution of traits. Mediodactylus geckos are distributed across the Balkan Peninsula, including the Aegean Sea islands and mainland Greece (Ajtić, 2014; Schwarz et al., 2016; Roll et al., 2017; Kotsakiozi et al., 2018). The closely related Mediodactylus kotschyi (Steindachner, 1870) and Mediodactylus oertzeni (Boettger, 1888) are widespread on Aegean islands and islets (Kotsakiozi et al., 2018). On the smallest islands, these geckos are often the only vertebrates present (Kassapidis et al., 2005; and YI, SM and RS personal observations). Each island is inhabited by only one species of Mediodactylus. The geckos vary greatly between islands in morphology, behaviour, diet, abundance and life history (Valakos, 1989; Valakos & Polymeni, 1990; Mollov, 2011; Slavenko et al., 2015; Schwarz et al., 2016; Itescu et al., 2017, 2018). This variation makes them excellent organisms with which to study the effects of island attributes on life-history traits. Geckos, a major reptilian radiation (> 1850 species; Uetz et al., 2019), usually lay only one or two eggs per clutch (Kratochvil & Kubicka, 2007). Population means, therefore, can vary between one (small clutch size, i.e. more instances of one-egg clutches) and two (large clutch size, i.e. more instances of two-egg clutches). We investigated the drivers of reproductive trait evolution in insular animals by studying a set of traits of multiple Aegean island populations of Mediodactylus geckos. We compared insular populations and tested how trait variation relates to several abiotic and biotic characteristics of the islands they inhabit. In comparison to other analyses, we used data from a large number of islands with similar history and climatic characteristics, but with highly variable areas, isolation and ecological communities. We tested multiple reproductive traits in a common garden design in the laboratory, which enabled us to test several competing hypotheses robustly. We predicted that insular populations would follow the ‘island syndrome’ (Adler & Levins, 1994). Thus, populations from small and remote islands would have evolved slow life histories compared with populations from islands where the fauna more closely resembles that of the mainland (i.e. large islands, close to the mainland). However, on islands that host nesting seabirds, we predicted a third strategy. Small islands often serve as nesting sites for seabirds. These, in turn, deliver ‘marine subsidies’, such as faecal material, food scraps and the decomposing carcasses of chicks and adult birds that enrich the islands with valuable nutrients (Polis & Hurd, 1996; Anderson & Polis, 1998; Paetzold et al., 2008). Studies of Aegean island reptiles have found that the presence of ‘marine subsidies’ influences lizards by selecting for increased reproductive effort (Pafilis et al., 2011; Slavenko et al., 2015). Thus, on islands with marine subsidies, we predicted that eggs and clutches would be larger and that laying would be more frequent, because resource availability is less limiting. Populations can thus become denser, and individuals can become larger and more aggressive, favouring large hatchlings (Pafilis et al., 2009). At the same time, more energy can be allocated to reproduction; therefore, clutches can be larger and frequent. MATERIAL AND METHODS Data collection We collected 310 gravid females of M. kotschyi and M. oertzeni from 31 Aegean islands (Fig. 1). Individuals were collected during May and June of 2015, 2016 and 2017 under a permit issued by the Greek Ministry of Environment and Energy (permit ΑΔΑ: ΩΜ4Χ4653Π8-2ΟΕ). We identified gravid females by observing the eggs through the semi-transparent skin of their abdomens (Slavenko et al., 2015: fig. 1). Upon capture, we measured and recorded the snout–vent length (SVL; to 0.01 mm precision, using Silverline 380244 callipers) of each female. We transported the females to the University of Athens, where they were housed in individual terraria and supplied with mealworms and water ad libitum, vitamins and calcium. Figure 1. Open in new tabDownload slide Map of islands sampled (red) during fieldwork seasons between May and June 2015–2017. Main panel: (1) Andros; (2) Mykonos; (3) Amorgos; (4) Sifnos; (5) Ios; (6) Karpathos; (7) Kassos. Inset A: (8) Skyros; (9) Exo Diavates. Inset B: (10) Paros; (11) Naxos; (12) Iraklia; (13) Venetiko; (14) Schinoussa; (15) Aspronissi; (16) Pano Koufounissi; (17) Glaronissi; (18) Antiparos; (19) Kato Fira; (20) Despotiko; (21) Tsimintiri; (22) Tourlos; (23) Preza; (24) Panteronissi; (25) Glaropounda. Inset C: (26) Anafi; (27) Megalo Fteno; (28) Mikro Fteno. Inset D: (29) Milos; (30) Kimolos; (31) Agios Eustathios. Figure 1. Open in new tabDownload slide Map of islands sampled (red) during fieldwork seasons between May and June 2015–2017. Main panel: (1) Andros; (2) Mykonos; (3) Amorgos; (4) Sifnos; (5) Ios; (6) Karpathos; (7) Kassos. Inset A: (8) Skyros; (9) Exo Diavates. Inset B: (10) Paros; (11) Naxos; (12) Iraklia; (13) Venetiko; (14) Schinoussa; (15) Aspronissi; (16) Pano Koufounissi; (17) Glaronissi; (18) Antiparos; (19) Kato Fira; (20) Despotiko; (21) Tsimintiri; (22) Tourlos; (23) Preza; (24) Panteronissi; (25) Glaropounda. Inset C: (26) Anafi; (27) Megalo Fteno; (28) Mikro Fteno. Inset D: (29) Milos; (30) Kimolos; (31) Agios Eustathios. Once the eggs were laid, we recorded their number and laying date, measured their length and width (to the nearest 0.01 mm) and incubated them in dedicated incubators (ReptiBator, digital egg incubator), in conditions (28 °C and 80% humidity) that were found to be highly suitable for them (Booth, 2004). We calculated the egg volume (V) using the prolate spheroid equation: V = 4/3πa2b, where a and b are half of the width and length of the egg, respectively (Arribas & Galan, 2005). We considered eggs laid by the same female within a period of ≤ 7 days as belonging to the same clutch (Stephen Goldberg, personal communication). Eggs laid over longer intervals were treated as belonging to different clutches (Supporting Information, Fig. S1). We then calculated clutch frequency as the number of clutches laid by all females of a population over a period of 5 months in captivity, divided by the number of females (thus, frequency is in units of clutch per season, where a season equals a 5 month period). We do not know whether the first clutch laid in the laboratory was the first clutch laid by the female during that season, but in the Aegean region these geckos are thought to start mating only at the end of April (Beutler & Gruber, 1979: 89), thus our estimation of clutch frequency seems reasonable. We collated data regarding geographical and ecological characteristics for each island. Island area and distance from the mainland were obtained from Itescu et al. (2018). We obtained data on distance from the nearest larger island from Itescu et al. (2019). We did not include temporal predictors, such as the time since separation from a larger landmass (island age), because this predictor is strongly correlated with island area in this land-bridge island system, where, for the most part larger islands separated first, and small islets separated from them. Moreover, Itescu et al. (2019) found that temporal isolation metrics were generally unimportant in explaining the variation in traits of Aegean reptiles, including Mediodactylus geckos. Richness of potential gecko predators (mammals, reptiles and birds; Supporting Information, Table S1) and the relative abundance of Mediodactylus were obtained from Itescu et al. (2017). We estimated relative abundance for five islands (Exo Diavates, Glaropounda, Preza, Tourlos and Skyros) not found in the dataset of Itescu et al. (2017) by repeating their protocol, i.e. counting the number of geckos found per hour of search by one of us (R.S.), during peak hours of activity and clear sky conditions. We also documented the presence of the javelin sand boa Eryx jaculus (Linnaeus, 1758) and the saurophagous nose-horned viper Vipera ammodytes (Linnaeus, 1758) on the islands from the literature (Valakos et al., 2008; Itescu et al., 2017) and by observing them on the islands. The former is known to prey on both adult lizards (mainly Podarcis) and their eggs (Cattaneo, 2010), and the latter on adult individuals (Itescu et al., 2017 and references therein). We did not include rodents in our list of potential predators, although mice and rats may prey on lizards or their eggs, because they are present on virtually all the islands in our dataset (Masseti, 2012). Although predator richness is the most common measure of predation pressure, it does not necessarily reflect predation intensity or efficiency (Jaksic & Busac, 1984; Itescu et al., 2017). We thus included three measures of predation (predator richness, viper presence and boa presence) to decipher how this important effect is best captured. On each island, we placed 21 dry pitfall traps (plastic cups with funnels, 10.8 cm in diameter and 10.1 cm in depth, 435 mL) 10 m apart in a random patch of natural phrygana (short Mediterranean scrubland; Diamantopoulos et al., 1994) habitat. We placed pitfalls ≤ 100 m away from where the lizards were collected. The islands were sampled during May and June of 2015, 2016 and 2017. Each island was sampled once. We assessed the amount of available food for each population by calculating the weighted average of terrestrial arthropod biomass collected after 48 h from these traps. Mediodactylus geckos were found to feed on terrestrial arthropods (Valakos & Polymeni, 1990), thus excluding flying insects from our sampling is reasonable. We estimated the number of nesting seabirds on islets upon reaching them, as a means of evaluating the amount of marine subsidies available on these islets. All predictor data are summarized in the Supporting Information (Table S2). Similar trait values may stem from shared ancestry (Darwin & Wallace, 1858). Kotsakiozi et al. (2018) recently proposed that the M. kotschyi complex, although monophyletic, should be split into five species, of which two, M. kotschyi and M. oerzeni, inhabit islands in our dataset. In order to correct for phylogenetic non-independence, we reconstructed a Bayesian inference phylogenetic tree of Mediodactylus populations using BEAST v.1.8.4 (Drummond et al., 2012). We used a concatenated dataset of three mitochondrial regions (16S, Cytb and COI) from 216 specimens (Supporting Information, Table S3) of Mediodactylus populations [M. kotschyi, M. oertzeni, Mediodactylus bartoni (Stepánek, 1934), Mediodactylus orientalis (Stepánek, 1937) and Mediodactylus danilewskii (Strauch, 1887)], collected from different localities in and around the Aegean Sea. Sequences for 174 individuals were retrieved from GenBank (from the studies of Kasapidis et al., 2005; Kotsakiozi et al., 2018). Forty-two individuals from islands not previously sampled for Mediodactylus were sequenced anew (Supporting Information, Table S3). Additional information, parameters and priors, along with the reconstructed phylogenetic tree, are presented in the Supporting Information (Fig. S2). Data analysis Data are fully accessible in Table 1 and as Supporting Information (Figs S1 and S2). All statistical analyses were conducted with R (R Development Core Team, 2013). To test our predictions concerning biotic and abiotic factors shaping insular population reproductive traits, we compiled a dataset including trait means of populations across islands (Table 1), and the attributes of the islands. When correcting for female size, we chose to use SVL, not mass, because mass may change rapidly and drastically after a meal or when the female is carrying eggs (Meiri, 2010). The SVL is thus usually a more reliable measure of size within and between populations of a species than mass. We performed a multiple regression analysis, with egg volume (log10-transformed) as the response and mother SVL, clutch size and clutch frequency as predictors, to test the relationship between the focal trait means. Table 1. Mean values of maternal snout–vent length and the studied reproductive traits egg volume, clutch size and clutch frequency Island . Egg volume (mm3) . . Clutch size . . Clutch frequency (clutches per female) . . Maternal snout–vent length (mm) . . . Mean . N . Mean . N . Mean . N . Mean . N . Agios Eustathios 353.0 23 1.3 21 1.9 11 45.35 11 Amorgos 412.1 11 1.3 10 1.7 6 46.94 6 Anafi 400.0 7 1.4 8 1.3 6 47.34 6 Andros 314.3 28 1.5 24 2.2 11 45.36 11 Antiparos 357.2 15 1.5 12 1.2 10 43.07 10 Aspronissi 385.1 9 1.4 7 1.2 6 46.97 6 Despotiko 287.6 28 1.6 29 1.9 16 43.31 16 Exo Diavates 326.0 17 1.4 16 1.6 10 47.36 10 Glaronissi 412.2 21 1.5 16 1.5 11 50.17 11 Glaropounda 358.0 13 1.0 14 1.6 9 44.45 9 Ios 394.2 16 1.3 12 1.3 9 43.36 9 Iraklia 374.5 24 1.6 15 1.5 10 45.77 10 Karpathos 262.1 21 1.6 16 1.8 13 40.49 9 Kato Fira 336.2 25 1.3 21 2.3 9 43.10 9 Kassos 297.8 19 1.4 15 1.5 13 40.73 10 Kimolos 403.5 10 1.3 12 1.7 7 43.89 7 Megalo Fteno 397.9 11 1.6 11 1.4 8 47.73 8 Mikro Fteno 401.5 9 1.4 11 1.4 8 47.39 8 Milos 409.0 18 1.4 13 1.6 8 45.43 8 Mykonos 357.9 19 1.7 12 1.3 9 45.80 9 Naxos 350.1 45 1.6 34 1.6 22 44.26 22 Pano Koufonissi 386.3 21 1.3 16 1.6 10 40.34 10 Panteronissi 370.7 12 1.1 11 1.6 5 46.74 5 Paros 335.0 66 1.4 61 2.2 36 44.13 36 Preza 376.4 22 1.2 19 1.7 10 44.04 10 Schinoussa 395.7 24 1.6 15 1.9 9 46.00 9 Sifnos 383.9 20 1.3 19 1.7 7 50.02 7 Skyros 295.0 13 1.7 11 2.7 7 48.10 7 Tourlos 355.0 19 1.3 18 1.6 8 45.29 8 Tsimintiri 311.5 20 1.1 19 2.3 13 44.45 13 Venetiko 335.8 18 1.4 14 1.5 9 41.71 9 Island . Egg volume (mm3) . . Clutch size . . Clutch frequency (clutches per female) . . Maternal snout–vent length (mm) . . . Mean . N . Mean . N . Mean . N . Mean . N . Agios Eustathios 353.0 23 1.3 21 1.9 11 45.35 11 Amorgos 412.1 11 1.3 10 1.7 6 46.94 6 Anafi 400.0 7 1.4 8 1.3 6 47.34 6 Andros 314.3 28 1.5 24 2.2 11 45.36 11 Antiparos 357.2 15 1.5 12 1.2 10 43.07 10 Aspronissi 385.1 9 1.4 7 1.2 6 46.97 6 Despotiko 287.6 28 1.6 29 1.9 16 43.31 16 Exo Diavates 326.0 17 1.4 16 1.6 10 47.36 10 Glaronissi 412.2 21 1.5 16 1.5 11 50.17 11 Glaropounda 358.0 13 1.0 14 1.6 9 44.45 9 Ios 394.2 16 1.3 12 1.3 9 43.36 9 Iraklia 374.5 24 1.6 15 1.5 10 45.77 10 Karpathos 262.1 21 1.6 16 1.8 13 40.49 9 Kato Fira 336.2 25 1.3 21 2.3 9 43.10 9 Kassos 297.8 19 1.4 15 1.5 13 40.73 10 Kimolos 403.5 10 1.3 12 1.7 7 43.89 7 Megalo Fteno 397.9 11 1.6 11 1.4 8 47.73 8 Mikro Fteno 401.5 9 1.4 11 1.4 8 47.39 8 Milos 409.0 18 1.4 13 1.6 8 45.43 8 Mykonos 357.9 19 1.7 12 1.3 9 45.80 9 Naxos 350.1 45 1.6 34 1.6 22 44.26 22 Pano Koufonissi 386.3 21 1.3 16 1.6 10 40.34 10 Panteronissi 370.7 12 1.1 11 1.6 5 46.74 5 Paros 335.0 66 1.4 61 2.2 36 44.13 36 Preza 376.4 22 1.2 19 1.7 10 44.04 10 Schinoussa 395.7 24 1.6 15 1.9 9 46.00 9 Sifnos 383.9 20 1.3 19 1.7 7 50.02 7 Skyros 295.0 13 1.7 11 2.7 7 48.10 7 Tourlos 355.0 19 1.3 18 1.6 8 45.29 8 Tsimintiri 311.5 20 1.1 19 2.3 13 44.45 13 Venetiko 335.8 18 1.4 14 1.5 9 41.71 9 Each mean value is presented next to the number of individuals on which it is based. Open in new tab Table 1. Mean values of maternal snout–vent length and the studied reproductive traits egg volume, clutch size and clutch frequency Island . Egg volume (mm3) . . Clutch size . . Clutch frequency (clutches per female) . . Maternal snout–vent length (mm) . . . Mean . N . Mean . N . Mean . N . Mean . N . Agios Eustathios 353.0 23 1.3 21 1.9 11 45.35 11 Amorgos 412.1 11 1.3 10 1.7 6 46.94 6 Anafi 400.0 7 1.4 8 1.3 6 47.34 6 Andros 314.3 28 1.5 24 2.2 11 45.36 11 Antiparos 357.2 15 1.5 12 1.2 10 43.07 10 Aspronissi 385.1 9 1.4 7 1.2 6 46.97 6 Despotiko 287.6 28 1.6 29 1.9 16 43.31 16 Exo Diavates 326.0 17 1.4 16 1.6 10 47.36 10 Glaronissi 412.2 21 1.5 16 1.5 11 50.17 11 Glaropounda 358.0 13 1.0 14 1.6 9 44.45 9 Ios 394.2 16 1.3 12 1.3 9 43.36 9 Iraklia 374.5 24 1.6 15 1.5 10 45.77 10 Karpathos 262.1 21 1.6 16 1.8 13 40.49 9 Kato Fira 336.2 25 1.3 21 2.3 9 43.10 9 Kassos 297.8 19 1.4 15 1.5 13 40.73 10 Kimolos 403.5 10 1.3 12 1.7 7 43.89 7 Megalo Fteno 397.9 11 1.6 11 1.4 8 47.73 8 Mikro Fteno 401.5 9 1.4 11 1.4 8 47.39 8 Milos 409.0 18 1.4 13 1.6 8 45.43 8 Mykonos 357.9 19 1.7 12 1.3 9 45.80 9 Naxos 350.1 45 1.6 34 1.6 22 44.26 22 Pano Koufonissi 386.3 21 1.3 16 1.6 10 40.34 10 Panteronissi 370.7 12 1.1 11 1.6 5 46.74 5 Paros 335.0 66 1.4 61 2.2 36 44.13 36 Preza 376.4 22 1.2 19 1.7 10 44.04 10 Schinoussa 395.7 24 1.6 15 1.9 9 46.00 9 Sifnos 383.9 20 1.3 19 1.7 7 50.02 7 Skyros 295.0 13 1.7 11 2.7 7 48.10 7 Tourlos 355.0 19 1.3 18 1.6 8 45.29 8 Tsimintiri 311.5 20 1.1 19 2.3 13 44.45 13 Venetiko 335.8 18 1.4 14 1.5 9 41.71 9 Island . Egg volume (mm3) . . Clutch size . . Clutch frequency (clutches per female) . . Maternal snout–vent length (mm) . . . Mean . N . Mean . N . Mean . N . Mean . N . Agios Eustathios 353.0 23 1.3 21 1.9 11 45.35 11 Amorgos 412.1 11 1.3 10 1.7 6 46.94 6 Anafi 400.0 7 1.4 8 1.3 6 47.34 6 Andros 314.3 28 1.5 24 2.2 11 45.36 11 Antiparos 357.2 15 1.5 12 1.2 10 43.07 10 Aspronissi 385.1 9 1.4 7 1.2 6 46.97 6 Despotiko 287.6 28 1.6 29 1.9 16 43.31 16 Exo Diavates 326.0 17 1.4 16 1.6 10 47.36 10 Glaronissi 412.2 21 1.5 16 1.5 11 50.17 11 Glaropounda 358.0 13 1.0 14 1.6 9 44.45 9 Ios 394.2 16 1.3 12 1.3 9 43.36 9 Iraklia 374.5 24 1.6 15 1.5 10 45.77 10 Karpathos 262.1 21 1.6 16 1.8 13 40.49 9 Kato Fira 336.2 25 1.3 21 2.3 9 43.10 9 Kassos 297.8 19 1.4 15 1.5 13 40.73 10 Kimolos 403.5 10 1.3 12 1.7 7 43.89 7 Megalo Fteno 397.9 11 1.6 11 1.4 8 47.73 8 Mikro Fteno 401.5 9 1.4 11 1.4 8 47.39 8 Milos 409.0 18 1.4 13 1.6 8 45.43 8 Mykonos 357.9 19 1.7 12 1.3 9 45.80 9 Naxos 350.1 45 1.6 34 1.6 22 44.26 22 Pano Koufonissi 386.3 21 1.3 16 1.6 10 40.34 10 Panteronissi 370.7 12 1.1 11 1.6 5 46.74 5 Paros 335.0 66 1.4 61 2.2 36 44.13 36 Preza 376.4 22 1.2 19 1.7 10 44.04 10 Schinoussa 395.7 24 1.6 15 1.9 9 46.00 9 Sifnos 383.9 20 1.3 19 1.7 7 50.02 7 Skyros 295.0 13 1.7 11 2.7 7 48.10 7 Tourlos 355.0 19 1.3 18 1.6 8 45.29 8 Tsimintiri 311.5 20 1.1 19 2.3 13 44.45 13 Venetiko 335.8 18 1.4 14 1.5 9 41.71 9 Each mean value is presented next to the number of individuals on which it is based. Open in new tab We then tested the influence of island characteristics on population means, using ANCOVA, with population means as the response variables. We tested both geographical models (examined predictors: island area, distance from the mainland and distance to the nearest larger island) and ecological models [examined predictors: Mediodactylus population density, potential predator richness, number of nesting seabirds, arthropod abundance and the presence vs. absence of two widespread potential gecko predators on Aegean Sea islands (V. ammodytes and E. jaculus; Cattaneo, 2010; Itescu et al., 2017; Supporting Information, Table S2]. We selected the best model by backwards stepwise model selection based on P-values (α < 0.05). A preliminary inspection of Akaike information criterion values across all possible models showed that in most cases, the best models were similar to models based on P-values. Discrepancies usually included models selected based on Akaike information criterion scores having more predictors, which were not in themselves statistically significant (results not shown; this is a well-known phenomenon, e.g. Arnold, 2010). We view these as mostly false-positive results and thus prefer to interpret the more conservative results based on P-values (in themselves often criticized as being too liberal criteria for assessing variable importance; Guthery, 2008). The predictor variables in each model were first tested for multi-collinearity. Variation inflation factors (O’Brien, 2007) never exceeded five, and thus we consider multi-collinearity negligible in our analyses. We also tested models with all predictors together against each response variable (egg volume, clutch size and clutch frequency) in turn. The results were qualitatively the same as those we obtained for the separate geographical and ecological models (Supporting Information, Table S4). The few discrepancies between the models can be attributed to the fact that in the model including all predictors together island area and predator richness had variation inflation factors exceeding five. We therefore decided to use area and predator richness in separate models, in order to prevent over-parameterization. To account for phylogenetic non-independence, we repeated all population-level analyses using phylogenetically corrected general least squares (PGLS) models (Freckleton et al., 2002), using the phylogenetic tree we constructed (Supporting Information, Fig. S2), computed with the R package ‘Caper’ (Orme et al., 2013). Most of the intraspecific relationships among the focal populations in the reconstructed tree were unsupported (bootstrap values < 0.95). Furthermore, the results of the PGLS analyses for egg volume were qualitatively similar to the ordinary least squares (OLS) model, and the phylogenetic signal of the PGLS model for clutch size and clutch frequency was zero. Therefore, we present the results of the non-phylogenetic models below. The full phylogenetic models are available in the Supporting Information (Table S5). RESULTS Trade-offs The mean values of the reproductive traits of each gecko population are presented in Table 1 and the Supporting Information (Table S6). Egg volume (log10-transformed) increased with mother SVL (intercept = 5.39 ± 0.32, slope = 0.03 ± 0.006, t = 3.50, P = 0.002), but decreased with mean clutch size (slope = −0.19 ± 0.09, t = −2.15, P = 0.04) and frequency (slope = −0.16 ± 0.05, t = −3.49, P = 0.002, N = 31, R2 = 0.53). This means that, corrected for female SVL, larger eggs are laid less frequently and in smaller clutches. This trade-off is most likely to result from constraints on female abdominal volume and physiology. Egg volume Across islands, mean egg volume (corrected for female SVL) increased by 24% for every 10-fold increase in distance from the mainland (Fig. 2A; Table 2A; Supporting Information, Table S4A) but with no other geographical predictor. Egg volumes were 2.2% higher in the presence of the boa, E. jaculus (Fig. 2B; Table 2B; Supporting Information, Table S4B). Egg volumes also increased by 0.7% with every extra gram of arthropod biomass and decreased by 0.7% with each additional predator species added (Table 2B; Supporting Information, S4B). Table 2. Summary of the best ordinary least squares multiple regression models for the reproductive traits egg volume, clutch size and clutch frequency as response variables and geographical (A) and ecological (B) predictors chosen via P-value . Egg volume . Clutch size . Clutch frequency . A. Geographical Maternal SVL + NS NS Log distance from mainland + NS − Log distance from larger landmass NS NS NS Log island area NS + NS B. Ecological Maternal SVL + NS NS Arthropod biomass + NS NS Mediodactylus gecko abundance NS NS NS Presence of nesting seabirds NS NS NS Potential predator species richness − + NS Presence of Eryx jaculus + − NS Presence of Vipera ammodytes NS NS NS . Egg volume . Clutch size . Clutch frequency . A. Geographical Maternal SVL + NS NS Log distance from mainland + NS − Log distance from larger landmass NS NS NS Log island area NS + NS B. Ecological Maternal SVL + NS NS Arthropod biomass + NS NS Mediodactylus gecko abundance NS NS NS Presence of nesting seabirds NS NS NS Potential predator species richness − + NS Presence of Eryx jaculus + − NS Presence of Vipera ammodytes NS NS NS The full model results are presented in the Supporting Information (Table S5A–E). Abbreviations: the +/− symbols indicate a positive or a negative correlation with a response variable, respectively; NS, predictors that were analysed but were not statistically significant in the best model; SVL, snout–vent length. Open in new tab Table 2. Summary of the best ordinary least squares multiple regression models for the reproductive traits egg volume, clutch size and clutch frequency as response variables and geographical (A) and ecological (B) predictors chosen via P-value . Egg volume . Clutch size . Clutch frequency . A. Geographical Maternal SVL + NS NS Log distance from mainland + NS − Log distance from larger landmass NS NS NS Log island area NS + NS B. Ecological Maternal SVL + NS NS Arthropod biomass + NS NS Mediodactylus gecko abundance NS NS NS Presence of nesting seabirds NS NS NS Potential predator species richness − + NS Presence of Eryx jaculus + − NS Presence of Vipera ammodytes NS NS NS . Egg volume . Clutch size . Clutch frequency . A. Geographical Maternal SVL + NS NS Log distance from mainland + NS − Log distance from larger landmass NS NS NS Log island area NS + NS B. Ecological Maternal SVL + NS NS Arthropod biomass + NS NS Mediodactylus gecko abundance NS NS NS Presence of nesting seabirds NS NS NS Potential predator species richness − + NS Presence of Eryx jaculus + − NS Presence of Vipera ammodytes NS NS NS The full model results are presented in the Supporting Information (Table S5A–E). Abbreviations: the +/− symbols indicate a positive or a negative correlation with a response variable, respectively; NS, predictors that were analysed but were not statistically significant in the best model; SVL, snout–vent length. Open in new tab Figure 2. Open in new tabDownload slide Main significant relationships obtained between the reproductive traits and predictors. A, mean egg volume (in cubic millimetres) vs. distance from the mainland (in kilometres). B, mean egg volume (in cubic millimetres) vs. mother snout–vent length (SVL; in millimetres) in the absence (red circles and continuous line) and presence (blue triangles and dashed line) of Eryx jaculus. C, mean clutch size vs. island area (in square kilometres). D, mean clutch size vs. predator richness (number of species) in the absence (red circles and continuous line) and presence (blue triangles and dashed line) of E. jaculus. E, mean clutch frequency (number of clutches per season) vs. distance from the mainland (in kilometres). Egg volume, distance from the mainland and island area are log10-transformed. The statistical models for these relationships are presented in the Supporting Information (Table S5). Figure 2. Open in new tabDownload slide Main significant relationships obtained between the reproductive traits and predictors. A, mean egg volume (in cubic millimetres) vs. distance from the mainland (in kilometres). B, mean egg volume (in cubic millimetres) vs. mother snout–vent length (SVL; in millimetres) in the absence (red circles and continuous line) and presence (blue triangles and dashed line) of Eryx jaculus. C, mean clutch size vs. island area (in square kilometres). D, mean clutch size vs. predator richness (number of species) in the absence (red circles and continuous line) and presence (blue triangles and dashed line) of E. jaculus. E, mean clutch frequency (number of clutches per season) vs. distance from the mainland (in kilometres). Egg volume, distance from the mainland and island area are log10-transformed. The statistical models for these relationships are presented in the Supporting Information (Table S5). Clutch size Clutch size was uncorrelated with female SVL, but increased by 11% for every 10-fold increase in island area (Fig. 2C; Table 2A; Supporting Information, Table S4C). Clutch size showed contrasting results with the presence of predators; it increased by 1% with each additional predator species added, but was 12% smaller on islands on which the oophagous boa E. jaculus was present (Fig. 2D; Table 2B; Supporting Information, Table S4D). Clutch frequency Clutch frequency decreased by 7.8% for every 10-fold increase in distance from the mainland (Fig. 2E; Table 2A; Supporting Information, Table S4G) and was uncorrelated with female SVL (i.e. smaller females laid as frequently as larger females; Supporting Information, Tables S3G and S4H). Clutch frequency was not correlated with any of the ecological predictors (Table 2A; Supporting Information, Table S4G). The distance to the nearest larger island, the Mediodactylus population density and the number of nesting seabirds were not correlated with clutch size, egg volume or clutch frequency (Table 2A, 2B). Discussion Our results generally supported some of the predictions of the theory of life-history evolution on islands. The effect sizes, however, were usually small, and some relationships remained equivocal. When examining the factors affecting reproductive traits across islands, it seems that spatial isolation plays a part in shaping life-history traits of insular geckos, although not always in the predicted direction. Egg volume evolution seems to follow some of the predictions of the ‘island syndrome’ (Adler & Levins, 1994), in that eggs are larger and are laid infrequently on distant islands. Thus isolation seems to be promoting slower life histories, as we predicted. Clutch size, likewise, is slightly larger on larger islands, as predicted by the ‘island syndrome’. This might be because on larger islands there are more predator species (intercept = −0.87 ± 0.17, slope = 0.24 ± 0.02, t = 12.35, P < 0.0001, R2 = 0.84, N = 31), which might increase predation pressure on the geckos. Consequently, this promotes a faster life history characterized by e.g. larger clutches, as we indeed found. Isolation and area are thought to influence life history through their effects on community diversity and composition (e.g. general species richness, competitor and predator richness and identity, resource abundance and population density) or by acting as proxies for other biotic or abiotic effects, such as precipitation. When attempting to quantify these factors directly, we generally found that they were either weakly or not at all associated with the life-history traits we examined. The effect of distance from the mainland on egg volume and clutch frequency in our study might be the result of another, unmeasured effect, such as precipitation, which scales with distance from the mainland. Unfortunately, as far as we can tell, no precipitation data exist at island-specific resolution (especially not for islands < 1 km2). Thus, we could not test the effect of precipitation directly. Although the distance from the mainland does not necessarily capture the vicariant nature of gene flow of M. kotschyi evolution on the Aegean islands, the alternative metric of spatial isolation, distance from the nearest larger island, proved uninformative. This is in agreement with Itescu et al. (2019), who found that mainland-related insularity indices were more strongly related to characteristics of insular populations than indices of isolation from neighbouring islands. Predation is considered to be an important driver of life-history traits across islands (Blumstein, 2002; Blumstein & Daniel, 2002). It seems that predator species richness, the most common (and straightforward to estimate) index of predation on islands (Pérez‐Mellado et al., 1997; Cooper et al., 2004; Pafilis et al., 2009; Itescu et al., 2017), drives faster life history on islands, promoting slightly larger clutches of somewhat smaller eggs, as predicted. The effect of predation, however, is neither simple nor straightforward when taking into account the presence of specific predators, which potentially prey on our study species (or their eggs). The presence of the boa E. jaculus seems to drive slower life histories in insular Mediodactylus (i.e. larger eggs and smaller clutches), contrary to the effect of predator richness. This is probably because predator richness is not correlated with predation intensity (Jaksic & Busack, 1984) or efficiency (Itescu et al., 2017). Eryx jaculus is known to prey on small rodents, fledgling birds, small lizards and lizard eggs (Bodenheimer, 1935; Gruber, 1989; Böhme, 1993; Rodríguez‐Robles et al., 1999; Cattaneo, 2010; Brock et al., 2015; Faraone et al., 2017) and will feed on adult geckos if they are the only available food (PP, personal observation). However, neither gecko adults nor eggs were identified in wild E. jaculus stomach contents (Cattaneo, 2010), and we have observed in the wild an E. jaculus individual and two adult geckos residing under the same log. If Mediodactylus eggs or adults are indeed eaten by this snake, our results are unexpected. Alternatively, E. jaculus might not affect geckos through direct predation, but rather through predation of rat pups (Rattus rattus). Rats occur on many Aegean islands (Brock et al., 2015), and they have been found to compose almost 30% of the stomach contents of wild E. jaculus individuals from, e.g. Ios, Naxos and Paros (Cattaneo, 2010). Rats may consume lizard eggs (Pérez-Mellado et al., 2008). The boa might thus reduce the predation pressure on gecko eggs imposed by rats, and thus facilitate a slower life history. Slavenko et al. (2015) found that the mean clutch size of M. kotschyi decreased with increasing island area, which contradicts the predictions of the ‘island syndrome’. They attributed this deviation to the presence of nesting seabirds having a beneficial effect on small island populations by the means of providing marine subsidies, which provide additional nutrients to the island biota. Slavenko et al. (2015) based their calculations of clutch size population means on count of eggs seen through the female abdomen. However, when we tested the difference between clutch size counted this way in the field it was higher than the number of eggs laid by the females in the laboratory (Student’s paired t-test, means: laboratory = 1.40 ± 0.02, field = 1.57 ± 0.03, N = 546, t = −5.78, P ≤ 0.0001). Thus, the differences between our results and those of Slavenko et al. (2015) might be attributed to our ability to quantify clutch sizes directly. Seabirds nest on 11 out of the 13 small islets (< 1 km2), uninhabited by humans, in our dataset. Arthropod abundance was not significantly different between small (< 1 km2) and larger islands (t-test: mean arthropod abundance on small islets = 3.6 ± 1.8 g, N = 13; mean on larger islands = 6.5 ± 1.1 g, N = 18; t = −1.4, P = 0.2) or between islands on which nesting birds are present or absent (t-test: mean arthropod abundance on islands on which seabirds are present = 4.1 ± 2.1 g, N = 11; seabirds absent = 6.0 ± 1.1 g, N = 20; t = −0.8, P = 0.4). Arthropod abundance was, likewise, not statistically different on small islets on which seabirds nest and on those without seabirds (t-test: nesting = 4.1 ± 2.1, N = 11; not nesting = 1.1 ± 0.05, N = 2; t = −1.4, P = 0.2). These results refute our predictions and also raise the question of whether nesting seabirds provide substantial marine subsidies and, if so, whether these are beneficial for arthropods and reptiles. It is also possible that the benefit that stems from marine subsidies is too short lived to influence the reproductive strategies of the local gecko population, owing to the transient nature of some seabird colonies across years. Arthropod abundance itself was, however, weakly (positively) correlated with egg volume, and thus seems to promote slower life histories, as predicted. The complex relationship between resource abundance and its effect on life-history traits remains, unfortunately, unexplained. We think that more direct examination of the effect of nesting seabirds on the ecology of small islands is warranted. We conclude that the factors that are commonly thought to affect life-history evolution on islands (i.e. island area, food availability, population density etc.) might not have a direct effect on life-history traits in some taxa. Thus, each species might evolve along different trajectories on different archipelagos, based on archipelago- and species-specific attributes and on contingency. Isolation and predation seem to play an important role in shaping life-history evolution on islands, at least in our study system. Our results imply that different measures of predation pressure might have different, and sometimes opposing, effects on life-history trait evolution. They thus highlight the importance of including specific predators, rather than only predator species richness, in analyses of trait evolution. The ‘island syndrome’ is probably not as general a pattern across insular faunas that it is sometimes claimed to be. SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article at the publisher’s website. Figure S1. Frequency distribution histogram of inter-clutch interval. Figure S2. Phylogenetic tree of Mediodactylus. Table S1. Potential predator species included in analysis. Table S2. Predictor variables per island. Table S3. Specimens included in the Mediodactylus phylogenetic tree. Table S4. Minimum adequate PGLS and OLS models. Table S5. PGLS and OLS model results of reproduction traits. Table S6. Averages and ranges of reproduction traits of Mediodactylus. ACKNOWLEDGEMENTS We thank Alison Gainsbury, Erez Maza, Alex Slavenko, Aviv Bejerano, Tamar Freud, Eden Goshen, Simon Jamison, Lama Khoury, Menachem Kurzits, Michael Mosses, Eylon Sharoni, Achiad Sviri, Oliver Tallowin, Johannes Foufopoulos, Ivan Monagan Jr, Sarah Semegen, Stephen Blake Graber, Johanna Fornberg, Alexandros Vezyrakis, Keren‐Or Wertheimer, David David, Sapir Rahamim and Gavin Stark for their valuable help with fieldwork. We thank Tamar Feldstein and the Steinhardt Museum of Natural History for extracting and sequencing DNA samples for ancestral tree reconstruction. We thank Gali Ofer for help with map construction. We thank three anonymous reviewers for their helpful comments. The study was funded by an Israel Science Foundation (ISF) grant #1005/12. The authors declare that there is no conflict of interest. REFERENCES Abboud RT , Wallace AM , English JC , Müller NL , Coxson H , Paré PD , Sandford AJ . 2006 . 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TI - Isolation and predation drive gecko life-history evolution on islands
JF - Biological Journal of the Linnean Society
DO - 10.1093/biolinnean/blz187
DA - 2020-02-28
UR - https://www.deepdyve.com/lp/oxford-university-press/isolation-and-predation-drive-gecko-life-history-evolution-on-islands-hUHFzavL5Z
SP - 618
VL - 129
IS - 3
DP - DeepDyve
ER -